Animal Behaviour Advantages Disadvantages No2

ANIMAL BEHAVIOUR: ADVANTAGES AND DISADVANTAGES NO.2 Kevin Brewer

ISBN: 978-1-904542-47-6

This document is produced under two principles: 1. All work is sourced to the original authors. The images are all available in the public domain (most from http://commons.wikimedia.org/wiki/Main_Page). You are free to use this document, but, please, quote the source (Kevin Brewer 2008) and do not claim it as you own work. This work is licensed under the Creative Commons Attribution (by) 3.0 License. To view a copy of this license, visit http://creativecommons.org/licenses/bync-nd/3.0/ or, send a letter to Creative Commons, 171 2nd Street, Suite 300, San Francisco, California, 94105, USA.

2. Details of the author are included so that the level of expertise of the writer can be assessed. This compares to documents which are not named and it is not possible to tell if the writer has any knowledge about their subject. Kevin Brewer BSocSc, MSc (http://kmbpsychology.jottit.com/) An independent academic psychologist, based in England, who has written extensively on different areas of psychology with an emphasis on the critical stance towards traditional ideas. Orsett Psychological Services, PO Box 179, Grays, Essex RM16 3EW UK [email protected]

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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CONTENTS Page Number 1. Advantages and Disadvantages of Inbreeding

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2. Advantages and Disadvantages of Monogamy

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3. Advantages and Disadvantages of Parental Care and Investment

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4. Advantages and Disadvantages of Lek Mating

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5. Advantages and Disadvantages of Non-Reproductive Sex in Animals

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Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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1. ADVANTAGES AND DISADVANTAGES OF INBREEDING 1.1. 1.2. 1.3. 1.4. 1.5.

Introduction Avoiding inbreeding Adaptations with inbreeding Amur leopards References

1.1. INTRODUCTION Inbreeding refers to matings among genetic relatives that reduces the variety of genes (an increase of homozygosity). "This could eventually lead to a 'mutational meltdown' for populations with an effective size ..of <100" (Keller and Waller 2002 p230). Inbreeding can be defined in a number of ways (Keller and Waller 2002):


Pedigree inbreeding - Both parents share ancestors, and the amount of inbreeding depends on the number of ancestors shared. An inbreeding coefficient (F) is calculated based on the probability of two genes at the same point on the chromosome being derived from the same gene in a common ancestor (known as "identical by descent"; IBD)(Keller and Waller 2002).




Inbreeding as non-random mating - This is the degree of relatedness of mates relative to two mates chosen at random in the population. An individual is inbred if its parents are more closely related than two individuals chosen at random.




Inbreeding because of population subdivision - Small isolated populations can be inbred even with random mating because of the choices are restricted.

Inbreeding produces two genetic threats - the accumulation of damaging mutations, and the random loss of certain genes. This produces a reduction in evolutionary fitness known as "inbreeding depression" (Keller and Waller 2002). For example, a higher rate of parasites and this reduced survival over winter in Soay sheep (Ovis aries) on a Scottish island (Coltman et al 1999). Crnokrak and Roff (1999) found statistically significant levels of inbreeding depression in 54% of species known to be inbred. Keller (1998) analysed the inbreeding coefficient of song sparrows on a Canadian island to quantify the Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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reduction in fitness. A mating between first degree relatives (eg: mother-son) reduced the hatching rate by around one-half, and this became three-quarters with two generations of such matings. While among baboons where males mate with females in natal troops (close genetic relatives including siblings), infant mortality was 100% in two studies, but none at al in another (table 1.1). SPECIES

FINDINGS

STUDY

Olive baboon (Papio anubis)(figure 1.1)

4/4 inbred vs 6/32 outbred infants died in first month

Packer (1979)

Yellow baboon (Papio cynocephalus)

3/3 inbred vs 27/140 outbred infants died in first month

Alberta and Altmann (1995)

Chacma baboon (Papio cynocephalus ursinus)

No difference in mortality between inbred and outbred infants up to three months old

Bulger and Hamilton (1988)

(After Pusey and Wolf 1996)

Table 1.1 - Three studies of baboon inbreeding and infant mortality.

(Source: US Fish and Wildlife Service; public domain)

Figure 1.1 - Olive baboon. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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Table 1.2 lists some of the criteria used and effects of inbreeding among birds, mammals, and poikilotherms (body temperature controlled by environment; eg: lizards) (Crnokrak and Roff 1999).

BIRDS

MAMMALS

POIKILOTHERMS



















Clutch/brood size Nestling survival Number of eggs hatched Number of young fledged Hatching success












Juvenile survivorship Probability of producing litter Litter size Juvenile weight Number of emergent young Percentage of emergent young Ejaculation volume Sperm motility Sperm abnormalities Body mass





Number of clutches Clutch size Hatching success Number of dead embryos Percentage fry survival Growth of adults

Table 1.2 - Criteria used to measure the effect of inbreeding in different species. Table 1.3 gives examples of studies showing effects of inbreeding in different animals.

ANIMAL

RISK

STUDY

Blue tit (Cyanistes caeruleus)

Reduced hatching rate

Kempenaers et al (1996)

Common shrew (Sorex araneus)

Survival to maturity; body length

Stockley et al (1993)

Harbour seal (Phoca vitulina)

Birth weight; neonatal survival

Coltman et al (1998)

Black-footed rock wallaby (Petrogale lateralis)

Fecundity (ie: amount of offspring)

Eldridge et al (1999)

(After Keller and Walter 2002)

Table 1.3 - Examples of studies on effect of inbreeding in a population. Table 1.4 gives some examples of studies showing specific inbreeding relationships in different animals.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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ANIMAL

RELATIONSHIP

FINDINGS

STUDY

Golden lion tamarin (Leonpithecus rosalia)

Fatherdaughter; siblings

14/14 inbred vs 1/5 outbred infants died before weaning

Dietz and Baker (1993)

Cooper's hawk (Accipiter cooperii)

Grandmothergrandson

Low hatching rate

Rosenfield and Bielefeldt (1992)

White-footed mice (Peromyscus leucopus noveboracensis)

Siblings

Lower survival rate when individuals born in captivity released into wild

Jiménez et al (1994)

(After Pusey and Wolf 1996)

Table 1.4 - Nature of inbreeding relationship and consequences in three studies. Though inbreeding has risks with "severely deleterious recessive alleles" 1 (Pusey and Wolf 1996)(figure 1.2), it can have advantages (table 1.5).

(Source: Imaginary Friend; public domain)

Figure 1.2 - Inbreeding and recessive gene example.

1

Allele is a possible copy of a gene at a particular point of the chromosome.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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ADVANTAGES 1. In small, isolated populations genetic relatives may be the only potential mates available. So it is better to mate with the risk for the offspring than to not mate at all. 2. Evolutionary advantages to inbreeding. In eusocial species, like ants, inbreeding is very high because only one female and a limited number of males mate. Among naked mole-rats (Heterocephalus glaber)(figure 1.3), that live in subterranean colonies in north-east Africa, "DNA fingerprinting" showed a mean relatedness of 0.81 (81%) (Reeve et al 1990). Altruistic behaviour becomes an advantage for individuals. Young from previous litters maintain the colony and raise the newborns. There is an evolutionary advantage to caring for siblings, who are genetically as similar, compared to having own offspring (50% similar to parents). 3. Choices limited for animals to seek non-relative mates including predator pressure, scarcity of food, and physical barriers to movement (Reeve et al 1990). 4. Risks of outbreeding including genetic incompatibility, pathogens, and mismatch between parents which limit parenting success (Pusey and Wolf 1996). Cohen and Dearborn (2004) reported that frigatebirds (Fregata minor) appeared to actively choose genetically similar mates (Box 1.1). DISADVANTAGES 1. Inbreeding depression; ie: reduced evolutionary fitness including sperm deformities, sterility, and decline in courtship frequency (Pusey and Wolf 1996). 2. Greater chance of young not surviving to adulthood; eg: inbred red-cockaded woodpeckers (Picoides borealis) in south-eastern USA have reduced hatching rates and fledgling survival (Daniels and Walters 2000). 3. Increased extinction risk, particularly for small populations, through reduced survival of young and shorter lifespan of survivors. 4. Reduced survivorship generally. A study of forty captive inbred populations showed an average increase in mortality of 33% compared to outbred populations (Ralls et al 1988). Jiménez et al (1994) followed the survival of captive-born White-footed mice (Peromyscus leucopus novaboracensis) over ten weeks after introduction to the wild at fields near Chicago Zoological Park, Brookfield, Illinois, USA. On average, survival of inbred mice was 56% that of non-inbred ones, mainly due to a greater loss of body mass by the former group. 5. Greater susceptibility to changes in the environment; eg: more inbred song sparrows (Melospiza melodia) died during storms on Mandarte Island, Canada (Keller et al 1994).

Table 1.5 - Advantages and disadvantages of inbreeding.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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(Source: Ltshears - Trisha M Shears; public domain)

Figure 1.3 - A naked mole-rat.

Great frigatebirds (figure 1.4) breed on remote islands in the Pacific and Indian Oceans, and show natal site fidelity (ie: breed close to where born) which is a risk factor for inbreeding. But on Tern Island (one of twelve small islands in the French Frigate Shoals atoll, northwestern Hawaiian islands, USA), where the population is studied, there is enough movement of males to counteract this risk (Cohen and Dearborn 2004). So if inbreeding occurs, it must be by female choice. Cohen and Dearborn (2004) collected blood samples for DNA fingerprinting from 92 family groups in 1998 and 1999. Genetic similarity between mates was greater than expected by chance (mean relatedness of 0.082; significantly different to zero) suggesting inbreeding. The authors concluded: "Although the potential for fitness consequences of this inbreeding remains unclear, the occurrence of inbreeding in this population is intriguing because it is likely to be the result of a active mate choice process" (p1234).

Box 1.1 - Details of Cohen and Dearborn (2004).

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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(Source: Jason Corriveau; in public domain)

Figure 1.4 - Male great frigatebird displaying. The benefits of inbreeding can be assessed in relation to two situations (Kokko and Ots 2006): a) Simultaneous choice scenario - Choice between incestuous and non-incestuous mating; b) Sequential choice scenario - Choice between mating with kin now or waiting for non-kin to appear. In the second situation, waiting for non-kin is risky because they may not appear or the individual may die before their arrival. So inbreeding makes sense in the sequential choice scenario. With the simultaneous choice scenario, inbreeding can make sense for the parent who cares for the offspring. A female who has a period of pregnancy and after-birth care is not able to mate again for a while. This is a "time out" (Kokko and Ots 2006). If such a female has mated with a related male, who then mates with unrelated females, she has gained indirect fitness from inbreeding. Indirect fitness refers to benefits at the level of the gene.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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1.2. AVOIDING INBREEDING 1. One way of avoiding inbreeding is through natal dispersion. At a certain time, juveniles are sent or choose to leave their group or site of birth. For example, male and female juvenile meadow voles (Microtus pennsylvanicus) were found to be more likely to disperse when released into a empty area with siblings than with non-siblings (Bollinger et al 1993). But dispersal has costs including predation risk, energy expenditure, inability to survive in new environments, and incompatibility with non-related mates. Thus some species choose mates of "intermediate relatedness" (Pusey and Wolf 1996). For example, female white-footed mice preferred to mate with unfamiliar first cousins than unfamiliar siblings or unfamiliar unrelated males (Keane 1990), and similarly Japanese quail females (Bateson 1982). Ekernas and Cords (2007) studied natal dispersion at between 6-8 years-old by young male blue monkeys (Cercopithecus mitis stuhlmanni) in the Kakamaga Forest, Kenya. Twenty-six natal dispersions were observed among three studied groups (each group ranging from thirtythree to sixty-five individuals). Four factors were analysed to explain the dispersal process: i) Dispersed males hounded out by adult males - This did not seem to be important as there was no difference in aggressive encounters between adult males and individuals who subsequently did or did not leave the group. ii) Dispersed males did not have mating opportunities - If this was the case, dispersion would occur during the mating season, and it did not more often than expected by chance. iii) Dispersed males have weaker social ties to the group - Dispersing and non-dispersing males did not vary in their social behaviour, but time spent in social activities (eg: grooming) was significantly greater for juvenile females compared to juvenile males. iv) Environmental factors involved - Male dispersal was more often during the dry season, and least likely when food was scarce. This would suggest that dispersion took place when the movers had a better chance of being accepted by the new group (ie: not during food shortages). Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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January was the month with the highest number of dispersals observed (n = 7), when rainfall was low and fruit availability generally high (table 1.6).

PERIOD

CHARACTERISTIC

NUMBER OF DISPERSALS

SIGNIFICANCE COMPARED TO CHANCE

May-Sept

Most conceptions

7

ns

Dec-Feb

Lowest average rainfall

16

more; p<0.0001

June-August

Food shortages

1

ns

Table 1.6 - Distribution of dispersals in three seasons. The authors felt that hormonal or biochemical changes associated with puberty played a role in triggering the process. In terms of inbreeding, the triggering process evolved to reduce the risk. Male spotted hyenas (Crocuta crocuta) leave the female socially dominated "clans". Höner et al (2007) analysed ten years of data on the hyena population of Ngorongoro Crater, Tanzania (370 individuals in eight clans), and found 90% of males dispersed. Females mate with several males which means that female offspring may not be able to recognise their genetic father, so they follow the rule: "avoid males that were members of your group when you were born and favour males that were born into or immigrated into your group after your birth" (p798). Data showed that 90% of litters were from males born into or immigrated into the female's group after her birth. Only two litters (of 309) were cubs from daughter-father matings. 2. Another way to overcome the risk of inbreeding is female extra-pair copulations with males from outside the natal group. For example, splendid fairy wrens (Malurus splendens) were estimated to have breeding pairs with close relatives in 25% of cases (compared to the average of 5% in other paired species; Pusey and Wolf 1996), but "DNA fingerprinting" showed evidence of eggs in the nest not sired by the resident male (Rowley et al 1993). 3. Kin recognition, through smell, for example, is important. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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Experiments place related individuals together or unrelated individuals to measure reproductive rates, which are lower among the related group, or individuals are offered a choice of mates of varying genetic relatedness. For example, wild house mice (Mus musculus) in sibling groups were less likely to produce litters compared to cousin groups or non-relatives (Krackow and Matsuschak 1991). While female mice given a choice of familiar siblings, non-familiar siblings, and nonsiblings preferred the latter for mating (Dewsbury 1988). 4. Delayed sexual maturation in the presence of close relatives; eg: marmosets and tamarins in the presence of opposite sex parents and siblings in their group. 1.3. ADAPTATIONS WITH INBREEDING In animals that show inbreeding, their behaviour may be different with kin - for example, ejaculating less sperm. Lewis and Wedell (2009) found that Indian meal moth (Plodia interpunctella)(figure 1.5) males ejaculated 54% less sperm when mating with sisters compared to unrelated females. These male moths transfer sperm to the female in a spermatophore, which contains the distinctively different fertile and non-fertile sperm. Sisters received significantly less fertile and non-fertile sperm (table 1.7). TYPE OF SPERM

RELATED FEMALES

UNRELATED FEMALES

Fertile

3000

4000

Non-fertile

30 000

45 000

Table 1.7 - Approximate mean number of sperm provided to unrelated and related females. Sperm production is costly for male moths who can mate only a handful of times (maximum eight; Ryne et al 2001) in their short lives (12 days average). Males also vary their ejaculation depending on the quality/fecundity of the female, and the presence of other males (sperm competition)(Lewis and Wedell 2009). But in red junglefowl (Gallus gallus), Pizzari et al (2004) found that males inseminated sisters with more sperm that unrelated females. This was because females have the ability to store sperm from multiple males and can "choose" which male's fertilises the eggs. This is a strategy for females to deal with the risk of inbreeding (Tregenza and Wedell 2002). Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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(Source: Kaldari; in public domain)

Figure 1.5 - Indian meal moth. 1.4. AMUR LEOPARDS The Amur (or Far Eastern) leopard (Panthera pardus orientalis) may be reduced to less forty wild individuals alive in the Russian Far East (Uphyrkina et al 2002). When a population is small the opportunities for breeding are limited, and this can lead to mating with close genetic relatives Inbreeding). Inbreeding increases the risk of recessive genes (those needing both copies of the gene to manifest the effect) and congenital problems Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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(eg: bone deformity). Also a decrease in litter size has been reported by field researchers (from two in 1973 to one in 1997)(Uphyrkina and O'Brien 2003). Uphyrkina and O'Brien (2003) found that wild Amur leopards from the Primorskiy Kray area of Russia and North Korea showed lower genetic variation than captive populations from zoos worldwide, and relatedness values of between 60-90% 2. The documentary, "The Last Leopard" (Director: Tatsuhiko Kobayashi), filmed Amur leopards in Kedrovaya Pad Natural Reserve, west of Vladivostok, Russia. The documentary reported genetic analysis of seven animals which showed inbreeding (figure 1.6).

Figure 1.6 - Genetic relationship between seven Amur leopards in Kedrovaya Pad Natural Reserve.

2

100% = identical twins; 50% = parent-offspring and between siblings.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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In figure 1.6, four matings are key: (i) Outbreeding. Two genetically unrelated individuals (Ugraty and Starshuka) mate and their offspring (Sbetlana and Puzan) will each share 50% of the genes of each biological parent. (ii) Inbreeding. The father (Ugraty) mates with his daughter (Sbetlana) producing female offspring (Marshuka). This gives a coefficient of inbreeding of 25%. This is the chance of getting two copies of a gene that are from the same ancestor. (iii) Inbreeding. Marshuka mates with her halfsibling (Puzan) to produce female offspring (Skrytnaya). Half-siblings normally share 25% of the same gene (and full siblings 50%). The coefficient of inbreeding is 12.5% here. (iv) Inbreeding. The father (Puzan) mates with his daughter (Skrytnaya) to produce cub 3. 1.5. REFERENCES Abbott, D.H (1993) Social conflict and reproductive suppression in marmoset and tamarin monkeys. In Mason, W.A & Mendoza, S.P (eds) Primate Social Conflict New York: State University of New York Press Alberta, S.C & Altmann, J (1995) Balancing costs and opportunities: Dispersal in male baboons American Naturalist 145, 279-306 Bateson, P (1982) Preferences for cousins in Japanese quails Nature 295, 236-237 Bollinger, E.K et al (1993) Inbreeding avoidance increases dispersal movements of the meadow vole Ecology 74, 1153-1156 Bulger, J & Hamilton, W.I (1988) Inbreeding and reproductive success in a natural chacma baboon Papio cynocephalus ursinus population Animal Behaviour 36, 574-578 Cohen, L.B & Dearborn, D.C (2004) Great frigatebirds, Fregate minor, choose mates that are genetically similar Animal Behaviour 68, 1229-1236 Coltman, D.W et al (1998) Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites Proceedings of the Royal Society of London B, Biological Sciences 265, 803-809 Coltman, D.W et al (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population Evolution 53, 1259-1267 Crnokrak, P & Roff, D.A (1999) Inbreeding depression in the wild Hereditary 83, 260-270 Daniels, S.J & Walters, J.R (2000) Inbreeding depression and its

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Details of conservation efforts at http://www.amur.org.uk/leopards.shtml and http://www.amurleopard.org/. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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effects on natal dispersion in red-cockaded woodpeckers Condor

102, 482-491

Dewsbury, D.A (1988) Kin discrimination and reproductive behaviour in muroid rodents Behavioural Genetics 18, 525-536 Dietz, J.M & Baker, A.J (1993) Polygyny and female reproductive success in golden lion tamarins, Leontopithecus rosalia Animal Behaviour 46, 1067-1078 Ekernas, L.S & Cords, M (2007) Social and environmental factors influencing natal dispersal in blue monkeys, Cercopithecus mitis stuhlmanni Animal Behaviour 73, 1009-1020 Eldridge, M.D.B et al (1999) Unprecedented low levels of genetic variation and inbreeding depression in an island population of the blackfooted rock wallaby Conservation Biology 13, 531-541 Höner, O.P et al (2007) Female mate-choice drives the evolution of male-biased dispersal in a social mammal Nature 448, 798-801 Jiménez, J.A et al (1994) An experimental study of inbreeding depression in a natural habitat Science 266, 271-273 Keane, B (1990) The effect of relatedness on reproductive success and mate choice in the white-footed mouse, Peromyscus leucopus Animal Behaviour 39, 264-273 Keller, L.F (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia) Evolution 52, 240-250 Keller, L.F & Waller, D.M (2002) Inbreeding effects in wild populations Trends in Ecology and Evolution 17, 5, 230-241 Keller, L.F et al (1994) Selection against inbred song sparrows during a natural population bottleneck Nature 372, 356-357 Kempenaers, B et al (1996) Genetic similarity, inbreeding and hatching failure in blue tits: Are unhatched eggs infertile? Proceedings of the Royal Society of London B, Biological Sciences 263, 179-185 Kokko, H & Ots, I (2006) When not to avoid inbreeding Evolution 3, 467-475

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Krackow, S & Matuschak, B (1991) Mate choice for non-siblings in wild house mice: Evidence from a choice test and a reproduction test Ethology 88, 99-108 Lewis, Z & Wedell, N (2009) Male moths reduce sperm investment in relatives Animal Behaviour 77, 6, 1547-1550 Packer, C (1979) Inter-troop transfer and inbreeding avoidance in Papio anubis Animal Behaviour 27, 1-36 Pizzari, T et al (2004) Sex specific, counteracting responses to inbreeding in a bird Proceedings of Royal Society of London, Series B 271, 2115-2121 Pusey, A & Wolf, M (1996) Inbreeding avoidance in animals Trends in Ecology and Evolution 11, 5, 201-206 Ralls, K et al (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals Conservation Biology 2, 185-193 Reeve, H.K et al (1990) DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole-rat Proceedings of the National Academy of Sciences, USA 87, 2496-2500 Rosenfield, R.N & Bielefeldt, I (1992) Natal dispersion and inbreeding in the Cooper's hawk Wilson Bulletin 104, 182-184 Rowley, I et al (1993) Inbreeding in birds. In Thornhill, N.W (ed) The

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives Chicago: University of Chicago Press Ryne, C et al (2001) Spermatophore size and multipl mating: Effects on reproductive success and post-mating behaviour in the Indian male moth Behaviour 138, 947-963 Stockley, P et al (1993) Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding Proceedings of the Royal Society of London B, Biological Sciences 254, 173-179 Tregenza, T & Wedell, N (2002) Polyandrous females avoid costs of inbreeding Nature 415, 71-73 Uphyrkina, O & O'Brien, S.J (2003) Applying molecular genetic tools to the conservation and action plan for the critically endangered far Eastern leopard (Panthera pardus orientalis) Comptes rendus-Biologies 326, S93-S97 Uphyrkina, O et al (2002) Conservation genetics of the Far Eastern leopard (Panthera pardus orientalis) Journal of Hereditary 93, 5, 303-311 (Freely available at http://jhered.oxfordjournals.org/cgi/reprint/93/5/303)

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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2. ADVANTAGES AND DISADVANTAGES OF MONOGAMY 2.1. 2.2. 2.3. 2.4.

Introduction Monogamy Monogamy and the vole Extra-pair copulations 2.4.1. Evaluation of Hill et al (1994) 2.5. Extra-pair copulations and apes 2.6. References 2.1. INTRODUCTION Monogamy involves mating (and often parental care) by one male and one female for a breeding season or for life. It is the form of social organisation found in about 3% of mammals (Young et al 1998), but in 15% of primates (Reichard 1995). The alternatives are polygamy (mating with multiple individuals who help in caring for the young), or promiscuity, which is multiple-partner matings without any post-copulation relationship. The best strategy will also vary between males and females (table 2.1). MALE 1. Monogamy: one partner for breeding season a. Mate-assistance monogamy

Male assists female in child-rearing

b. Mate-guarding monogamy

Female dispersal

2. Polygyny: one male with multiple females a. Female defence polygyny

Male defends cluster of females

b. Resource defence polygyny

Male defends resources and females come

c. Lek polygyny

Male defends territory and females come to mate only

d. Scramble competition polygyny

Males find scattered females

FEMALE 1. Monogamy a. Female-enforced monogamy

Male keeps other females away and assists in childrearing

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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2. Polyandry: one female with multiple males a. Fertility-insurance polyandry

Greater fertilisation of eggs

b. Better sperm polyandry

Genetically diverse sperm

c. More material benefits polyandry

More resources from males

d. More paternal care polyandry

More males help in child-rearing

(After Alcock 1993)

Table 2.1 - Types of mating strategy. The best strategy for passing the genes into the next generation will vary between the male and female of the species. The male is able to produce many sperm, and so can theoretically have as many offspring as mates found. But the female is restricted, in most species, by giving birth to the offspring. Thus she has more invested in its survival (table 2.2). Different species behave in different ways depending upon their environments, but generally the example in table 2.2 is the common strategy of sexual selection. "Female choosiness" has led to the evolution of males who compete, in some way, to show the female that their genes are best for mating. This competition involves fights, "shows of quality" (eg: ornaments like a peacock's tail), or the collection of scare resources to give to the female ("resource-holding power"; RHP). EXAMPLE - Male mates with ten females, who have one offspring each in the breeding season OFFSPRING

STRATEGY

MALE

10 fathered; can afford some not to survive

Find many female mates; ie: indiscriminate; little concern for post-natal care

FEMALE

Each female has one offspring and thus survival important

Female invests time and effort in survival, but must exercise choosiness about male; ie: only mate with male who has "best genes"

Table 2.2 - Sexual selection and strategies for males and females. Table 2.3 shows the factors that influence mating Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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strategies. WHY MALE STAYS 1. 2.

WHY FEMALE STAYS

WHY ONE MALE

WHY ONE FEMALE

WHY WHY MALE FEMALE EXCLUSIVE EXCLUSIVE

X X

3.

X

4.

X

5.

X

6.

X

7. 1 2 3 4 5 6 7

= = = = = = =

X

X

X

X X

X

X

X X

X

Matneral care needed Paternal care needed Geographical distribution of breeding females eg sparse Geographical distribution of breeding males Resource distribution eg limited Male-male aggression Female-female aggression

(After Gowaty 1996)

Table 2.3 - Factors influencing mating strategies. 2.2. MONOGAMY There are different types and explanations of monogamy including obligate and facultative (Kleitman 1977). The former relates to the need of the offspring to be cared for by both parents. Facultative monogamy is where males cannot monopolise more than one female because the females are geographically dispersed (Komers and Brotherton 1997). Komers and Brotherton (1997) compared these two types of monogamy in different mammal species. "Paternal care was considered to be present if males of that species are known to retrieve young, transport young, or provide food" (p1261). Monogamy was found to exist significantly more often in the absence of parental care than in the presence of it. "For a general theory on the evolution of monogamy in mammals, we must therefore focus on factors other than paternal care that may have promoted monogamy" (Komers and Brotherton 1997 p1267). Monogamy was also not common in species with geographically dispersed females, but it was more common where females were solitary living in small, exclusive territories that males could monopolise. Staying with one female reduced the risk and costs for Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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males of searching for multiple females. Table 2.4 summarises the main advantages and disadvantages of monogamy. ADVANTAGES 1. Know quality of partner and their genes. 2. Usually help with rearing young, which is crucial when biparental care is required. 3. Less risk of female-female and male-male aggression compared to polygamy. 4. A strategy that can be short-term (one breeding season) or longterm (for life). 5. Less risk of infanticide than with polygamy. 6. Best strategy for males if females are geographically dispersed and/or scarce. 7. Males can be certainty of their paternity compared to polyandry. DISADVANTAGES 1. Fear of extra-pair copulations, and males, in particular, end up caring for non-genetic offspring. 2. Lack of variety of genes over multiple breeding seasons. 3. If male partner infertile, for example, female will be unfertilised. 4. Cost of mate-guarding for males. 5. If no mate than no breeding that season. 6. Often involves courtship and displays which have costs. 7. Limits to amount of offspring per breeding season, particularly for males, compared to polygamy.

Table 2.4 - Advantages and disadvantages of monogamy. Where animals are monogamous, there is usually a complex system of courtship - a series of tests for males to show to the females their commitment to her and the care of the young as well as the quality of their genes (table 2.5). 1. Ensures pairing with the right species 2. Permits survival in aggressive species; ie: to approach without being attacked 3. Display of fitness 4. Improves species; ie: only fittest survive

Table 2.5 - Functions of courtship. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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Potential mates have to "establish clues to species identification, genetic superiority, and complementarity to the selecting individual, and for species with parental care, the quality and quantity of care an individual is likely to provide" (Burley 1981 p515). So in many species, it is possible that multiple criteria are used for mate selection. Burley (1981) compared mate choice by pigeons using three sets of criteria: i) Plumage colour ("blue" or "ash-red") and pattern ("checker" or "bar"); ii) Age and reproductive experience - "Superexperienced (eight or more clutches), "semi-experienced (1-2 clutches), or "no experience. (Experience leads to more efficient breeding (eg: fledge heavier young), but a reduced breeding rate; iii) Relative dominance position - Preference for dominant individuals or individuals of the same rank. The preference for these different characteristics was tested by giving a pigeon ("chooser") a choice of two opposite-sex birds with differences in specific ways. Table 2.6 summarises the findings in the choice tests.

MALE PREFERENCES

FEMALE PREFERENCES

Plumage

Blue over ash-red

Blue checker over blue bar; blue bar over ash-red bar or checker

Age and experience

More experienced; experience more important than age; Less experienced young over super-experienced old

More experienced; experience more important than age; Less experienced young over superexperienced old

Dominance

No preferences

Experienced females preferred dominant males; inexperienced females no preference

Table 2.6 - Preferences by pigeons on choices of individual characteristics. All the individual preferences were combined into a selectivity index, which showed that females were more selective than males. This fits with the prediction that the sex who makes the greater parental investment will be more selective (Trivers 1972); ie: females in monogamy. However, Burley (1981) admitted that selectivity is Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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not necessarily constant over time, and may vary with length of time since heterosexual contact, and season. For example, with the latter, males had stronger preferences in August-October than in January-March. 2.3. MONOGAMY AND THE VOLE The vole of North America is interesting to study in relation to social organisation because different species show completely different behaviours. The prairie vole (Microtus ochrogaster)(figure 2.1) is monogamous, while the montane vole (Microtus montanus) is promiscuous (table 2.7).

PRAIRIE VOLE

MONTANE VOLE

Mating system

Monogamy

Promiscuous

Parental care

Both parents involved in prolonged care of offspring

Mother only, but even she abandons young soon after birth

Behaviour

High level of social contact as species (50% of time in contact in experiments). Paired males aggressive towards other members of species

Low level of social contact (5% of time). Live in isolated burrows.

Table 2.7 - Differences in social organisation between two species of voles.

(Source: US National Park Service; in public domain)

Figure 2.1 - Prairie vole. The difference between the two species of voles has been explained by the hormones, oxytocin and vasopressin. Oxytocin triggers maternal behaviour, and partner preference in female prairie voles. While vasopressin triggers paternal care, and partner preference in male prairie voles (Young et al 1998). Research has shown that in prairie voles copulation Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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triggers oxytocin release because where it is blocked by drugs, the female does not stay with the male after mating (Williams et al 1994). The prairie vole brain has oxytocin receptors in areas in the brain related to reward (mesolimbic dopamine reward pathway) which conditions the female to the odour of her mate. The montane vole has less such receptors (Young et al 1998). Injections of oxytocin in unmated females and vasopressin in unmated males produces a preference for cagemates (Young et al 1998). But injections of vasopressin into male montane voles produced increased autogrooming only (Young et al 1997). 2.4. EXTRA-PAIR COPULATIONS Sexual selection explains the different strategies by males and females of a species when looking for a mating partner. For example, female choosiness leads to the evolution of males who can display their good quality genes in obvious ways, like the strength of calls or visual "ornaments", or males who provide resources to support the female during pregnancy and after birth. In a polygynous system, where females mate with multiple males, sexual competition among males will be high. But in monogamous species, partner choice may be limited and so it is better to have any mate than not breed. However, female extra-pair copulation (EPC) widens the choice of genes, particularly if the male breeding partner has low quality genes (Hill et al 1994). So males need still to signal their quality of genes. For example, male barn swallows with longer tail streamers (signal of good genes) engage in more EPCs than short-tailed males (Moller 1988). Where male care is essential, this will influence females from seeking EPCs (figure 2.2). MALE CARE ESSENTIAL ↓ FEMALE EPC COST = LOSS OF MALE CARE ↓ FEMALE DON'T SEEK EPC ↓ EXTRA-PAIR PATERNITY (EPP) RARE ↑ NO SELECTION PRESSURE ON MALES AS EPC PARTNER

MALE CARE NOT ESSENTIAL ↓ NO OR LOW EPC COST ↓ FEMALE SEEKS EPC ↓ EPP OCCURS ↑ STRONG SELECTION PRESSURE ON MALES AS EPC PARTNER

(After Birkhead and Moller 1996)

Figure 2.2 - Females seeking extra-pair copulations. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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Hill et al (1994) investigated female EPC among house finches (Carpodacus mexicanus)(figure 2.3) in one breeding season (1991) at the University of Michigan, Ann Arbor, USA. The bright plumage of the males is an "honest signal" of gene quality and parental investment. Males with brighter plumage have been observed to feed incubating females more than males with dimmer plumage (Hill 1991).

(Source: Public domain)

Figure 2.3 - Male house finch. Hill et al scored the plumage brightness 4 of both sexes on seven areas of the body (four on the underside, crown, eyestripe, and rump) to give a single index of overall plumage brightness. Blood samples were also taken for "DNA fingerprinting" to establish paternity. Broods from thirty-five nests were analysed (n = 119 chicks). It was expected that males with dull plumage will be cuckolded more. Ten chicks (8.4%) in five different nests were clearly fathered by a male other than the attending male at the nest. There was no difference in plumage brightness scores, wing length, and age of cuckolded and non-cuckolded males. The results were not as expected, and the only variable showing a significant difference

4

The plumage colour varies from pale yellow to bright red (Hill 1992).

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was nest dispersion - all illegitimate nestlings were in closely dispersed nests. If there is no difference in plumage brightness and cuckoldry, the authors asked, why would bright plumage evolve in male house finches. One answer is that there are more males than females (sex ratio of 1.52 males to one female), and so males are competing to find a mate. Also brighter plumage males mate earlier in the breeding season (by as much as 100 days at the extremes), and this would allow more broods per season. 2.4.1. Evaluation of Hill et al (1994) 1. Most of the birds were captured in traps or mist nets (figure 2.4) in order to fit with coloured leg bands for identification purposes. Though this is a common practice, what is the effect upon the birds?

(Source: Julio Reis)

Figure 2.4 - Bird trapped in mist net. 2. The overall plumage brightness index score was based on adding 21 individual scores together - seven regions of the body and scores for hue, intensity, and tone 5 for each as compared to colour slides in the "Methuen Handbook of Colour" (Kornerup and Wanscher 1983). The reliability of such a score could be open to question. 3. The effect on the birds of taking a blood sample. The chicks were sampled 8-10 days after hatching. 4. The authors admitted: "Date of capture is potentially important in a study of paternity. If a female or her mate is detained during the female's fertile period, observer-induced EPCs may result. Most birds in this study were sampled before the start of nest-building or after egg-laying was complete when handling should not have affected paternity. However, a few males and females were just captured just prior to or during egg-laying, so we also looked for an effect of capture date on

5

Hue scores ranged from colourless (1) through yellow (2-4), orange (5-8), to red (9-11). Intensity was scored from 1 to 8, and tone from 1 to 6 (Hill 1992). Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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cuckoldry" (Hill et al 1994 p194). 5. Standard procedures of the time were used for "DNA fingerprinting" and thus calculating paternity. However, the cost of the process was high and this limited the sample size of the study. 6. One-tailed tests were used for statistical analysis as a clear prediction of duller plumage males experiencing more cuckolds was made (one-tailed research hypothesis). One-tailed tests have less risk of a Type I error (claiming a significant result when the findings were due to chance; ie: non-significant). 7. The differences between cuckolded and non-cuckolded males were statistically analysed with the Mann-Whitney U test (table 2.8). This test was used because the plumage brightness index score can be classed as ordinal data, and thus a parametric statistical test could not be used. The Mann-Whitney test is ideal for comparing groups of different sizes (table 2.9). COMPARISON

"U" VALUE

PROBABILITY

SIZE OF GROUPS (N)

CRITICAL VALUE*

Plumage brightness score

62

0.44

5, 26

27

Wing length

40.5

0.11

5, 25

27

Female plumage colouration

29.5

0.30

5, 17

17

Clutch initiation date

55

0.59

5, 26

27

Clutch size

41.5

0.30

5, 23

24

Male age

56

0.31

5, 26

27

(* = U value must be less than critical value to be significant. Critical values taken from Coolican 1990).

Table 2.8 - Non-significant results from Mann Whitney tests comparing cuckolded and non-cuckolded males.

ADVANTAGES

DISADVANTAGES

1. Does not need groups to be of equal size.

1. Not as efficient as parametric tests.

2. Good with small samples.

2. Deals with relative positions not absolute scores.

3. Not restricted by parametric criteria.

3. Problems if too many tied

Table 2.9 - Main advantages and disadvantages of the Mann Whitney U test. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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8. The sample size of cuckolded males was low (n = 5) which could mean that there is low statistical power in the statistical analysis. This means that the statistical test is limited in its ability to find a significant difference in the data. 9. The means of the plumage brightness scores were used, whereas the median may have been better (table 2.10).

MEAN

MEDIAN

Definition

Add up scores and divide by number of scores.

Put data into order and take middle number.

Advantages

1. Most sensitive measure of central tendency.

1. Shows exact middle point with 50% above/below.

2. Total and all values taken into account.

2. Unaffected by extreme values in one direction.

1. Not good if extreme scores or scores vary greatly as with small samples.

1. Less information used than the mean.

Disadvantages

2. Time consuming to rank large sets of data.

2. Not good with highly skewed distributions.

Table 2.10 - Mean and median as measures of central tendency. 10. The differences were presented graphically with boxplots, which show the distribution of the scores with 10th, 25th, 50th, 75th and 90th percentiles. However, this can be distorted by the small number of cuckolded males (table 2.11).

10th 25th 50th 75th 90th

MALE PLUMAGE BRIGHTNESS SCORE NON-CUCKOLDED* CUCKOLDED*

MALE AGE (YEARS) NON CUCKOLDED

120 135 145 153 157

1.0 1.0 2.0 3.0 4.0

133 141 144 150 150

1.0 1.0 2.0 4.1 4.6

(* n = 26; ** n = 5) (After Hill et al 1994)

Table 2.11 - Distribution of scores from box-plots of cuckolded and non-cuckolded males.

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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2.5. EXTRA-PAIR COPULATIONS AND APES Reichard (1995) reported EPCs among three families of white-handed gibbons (Hylobates lar)(figure 2.5) observed in Khao Yai National Park,Thailand (table 2.12). GROUP

SIZE

ADULT MALE

ADULT FEMALE

A

4

Fearless

Andromeda

B

5

Bard

Bridget

C

6

Cassius

Cassandra

Table 2.12- Details of three family groups observed by Reichard (1995).

(Source: Ltshears)

Figure 2.5 - White-handed gibbon. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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Among these long-term monogamous primates, observed daily for nearly eighteen months between January 1992 to August 1993, three EPCs were witnessed: Andromeda and Cassius twice, and Andromeda and Bard. Reichard's field notes described the last occasion thus: " [0645h] Immediately, a copulation in a dorso-ventral position followed. It lasted only a few seconds, because [Fearless] - who probably detected the EPC - charged towards the couple and vigorously pursued the escaping [Bard] for more than 30 minutes" (p106). The EPCs were only 12% of all copulations observed by Reichard (1995), the majority were with the paired male (76 of 82). Though the female may gain other genes from an EPC, there is a risk of injury in the activity and her partner may then seek EPCs (table 2.13). The evolutionary response to female EPCs for males is mateguarding and retention behaviour.

ADVANTAGES

DISADVANTAGES

1. To gain better genes.

1. Risk that male partner will engage in EPC.

2. To gain a variety of genes, particularly if inbreeding involved.

2. Risk that partner may leave offspring (mate desertion).

3. To increase sperm competition and consequently reproductive rate.

3. Risk of injury during EPC.

4. To lower the risk of infanticide if EPC male becomes mate.

5. Risk of diseases and pathogens.

4. Risk of injury from mate.

5. The fear of EPC can encourage the mate to copulate more, and mate-guarding behaviour.

Table 2.13 - Advantages and disadvantages of EPCs for females in monogamous species. The Reichard (1995) study is an example of a naturalistic observation over a long period by the researcher, which collects qualitative data (that can be converted into quantitative data later). This type of study has advantages and disadvantages (table 2.14).

Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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ADVANTAGES

DISADVANTAGES

1. Very detailed study of gibbons over long periods of time.

1. Depends upon the observer; ie: information may be missed because of the focus on one event or that it takes place outside the observer's field of view.

2. All observations are recorded for later analysis. 3. The observer is able to recognise individual animals and record their behaviour.

2. The animals were well habituated to human observers, but does the presence of such observers change the gibbons' behaviour? 3. Very time consuming for the researcher.

Table 2.14 - Advantages and disadvantages of Reichard's (1995) naturalistic observation method. In a similar study of white-handed gibbons and siamang (Hylobates syndactylus)(figure 2.6) over 2.5 years at the Ketambe Research Station, Sumatra, Indonesia, Palombit (1994) observed five episodes of EPC. These involved a female siamang mating with three males from a neighbouring group at different times (table 2.15).

EPC WITH:

DATE

Immature male of P group (3 times)

15 February 1986 7 August 1986 26 September 1986

Adult male: mate of P group

9 April 1986

New adult male: mate of P group

9 February 1987

Table 2.15- Five EPCs by female siamang from C group. The "C" female "played a role in initiating them by: (1) maintaining proximity to the territorial border where a male from a neighbouring group could gain sexual access to her (which sometimes involved moving towards the male); (2) not avoiding an extra-group male that approached her; and (3) directing the.. 'solicitation' gesture at some extra-group males.." (p722). This female may have been motivated to find EPCs because she produced a premature stillborn and no other offspring during the study.

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(Source: Vassil; in public domain)

Figure 2.6 - Siamang. In both this study and Reichard (1995), the EPCs were rare, but it does not mean "that they are of negligible evolutionary importance if only for the reason that observations of sexual behaviour ..in general are extremely limited for wild ..siamang.. in part because of the typically long intervals between periods of female receptivity" (Palombit 1994 p722). Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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2.6. REFERENCES Alcock, J (1993) Animal Behaviour (5th ed) Associates

Sunderland, MA: Sinauer

Birkhead, T & Moller, A.P (1996) Monogamy and sperm competition. In Black, J.M (ed) Partnerships in Birds Oxford: Oxford University Press Burley, N (1981) Mate choice by multiple criteria in a monogamous species American Naturalist 117, 515-528 Coolican , H (1990) Research Methods and Statistics in Psychology London: Hodder & Stoughton Gowaty, P.A (1996) Battle of sexes and origins of monogamy. In Black, J.M (ed) Partnerships in Birds Oxford: Oxford University Press Hill, G.E (1991) Plumage colouration is a sexually selected indicator of male quality Nature 350, 337-339 Hill, G.E (1992) Proximate basis of variation in carotenoid pigmentation in male house finches Auk 109, 1, 1-12 Hill, G.E et al (1994) Sexual selection and cuckoldry in a monogamous songbird: Implications for sexual selection theory Behavioural Ecology and Sociobiology 35, 193-199 Kleitman, D.G (1977) Monogamy in mammals Quarterly Review of Biology 52, 39-69 Komers, P.E & Brotherton, P.N.M (1997) Female space use is the best predictor of monogamy in mammals Proceedings of the Royal Society of London B 264, 1261-1270 Kornerup, A & Wanscher, J.H (1983) Methuen Handbook of Colours London: Methuen Moller, A.P (1988) Female choice selects for male sexual trait ornaments in the monogamous swallow Nature 322, 640-642 Palombit, R.A (1994) Extra-pair copulations in a monogamous ape Animal Behaviour 47, 721-723 Reichard, U (1995) Extra-pair copulations in a monogamous gibbon (Hylobates lar) Ethology 100, 99-112 Trivers, R.L (1972) Parental investment and sexual selection. In Campbell, B (ed) Sexual Selection and the Descent of Man Chicago: Aldine Williams, J.R et al (1994) Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster) Journal of Neuroscience 6, 247-250 Young, L.J et al (1997) Species differences in V1a receptor gene expression in monogamous and non-monogamous voles: Behavioural consequences Behavioural Neuroscience 111, 599-605 Young, L.J et al (1998) Neuroendocrine basis of monogamy Trends in Neuroscience 21, 2, 71-75

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3. ADVANTAGES AND DISADVANTAGES OF PARENTAL CARE AND INVESTMENT 3.1. 3.2. 3.3. 3.4.

Introduction Prolonged parental care Red deer and sex of offspring References

3.1. INTRODUCTION The patterns of parental care (table 3.1) vary between species based on the amount of parental investment by each sex. "Investment" is seen as anything done by a parent to increase the chances of the survival of that particular offspring, which is at the expense of the parent's ability to invest in future offspring (Trivers 1972). Thus the parent who has invested more tends to care for that offspring, while the parent with the least investment may desert.







Both parents (biparental); Female only; Male only (sex role reversal); No care - offspring left to fend for themselves immediately after hatching or birth; Alloparental care - care by individuals (usually genetically related) but not genetic parents; eg: eusocial insects; Brood parasitism - fostering (care by genetic non-relatives); ie: placing eggs in nest unnoticed in case of cuckoo.

Table 3.1 - Types of parental care. There are a number of parental care decisions and thus mating strategies (table 3.2). FEMALE STAYS AFTER BIRTH

FEMALE LEAVES AFTER BIRTH

MALE STAYS AFTER BIRTH

Equal investment by both partners; monogamy

Male greater investment than female; sex-role reversal

MALE LEAVES AFTER BIRTH

Multiple partners for male; female greater investment than male

Multiple partners for male; many eggs must survive

Table 3.2 - Different parental care decisions and mating strategies. Maynard Smith (1977) viewed the relationship between Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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the parents as a "game" (as in "game theory") - an assessment of costs and benefits of staying or deserting (table 3.3). AMOUNT OF INVESTMENT:

FEMALE MORE THAN MALE

MALE MORE THAN FEMALE

EQUAL

WHO CARES FOR YOUNG:

MALE

FEMALE

JOINT/BOTH DESERT

Table 3.3 - Strategies for parental care based on parental investment. The decision to desert or stay and care for the offspring depends on a number of factors (Maynard Smith 1978):


Effectiveness of parental care by one vs two parents.




The chances of the deserter being able to mate again.




The security of paternity for the male.




The age of the offspring.




Whether fertilisation is internal or external. External fertilisation in many species of fish, for example, leads to males care for the eggs (table 3.4). FERTILISATION INTERNAL MALE FEMALE BOTH 28 6 8

FERTILISATION EXTERNAL MALE FEMALE BOTH 2 10 0

(After Breder and Rosen 1966)

Table 3.4 - Number of species of bony fishes where different parents care for offspring based on type of fertilisation. 3.2. PROLONGED PARENTAL CARE In species that care for the young, that caring stops when the offspring is a certain age (eg: fledgling that leaves the nest in birds). In many cases, the young leave the home in the process known as natal dispersion. But there are exceptions noted, particularly among birds, in the case of "co-operative breeding". This is where young from previous years aid the parents in raising this year's offspring through feeding or defence of the nest. Other species of birds, like swans, provide prolonged parental care (PPC) after the young can feed themselves. The reason may include guiding the offspring Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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on the first migration. Scott (1980) investigated PPC by Bewick's swans (Cygnus columbianus bewickii)(figure 3.1) wintering at the Wildfowl Trust Refuge, Welney, Norfolk, UK. It has been suggested that PPC protects the offspring from aggression during feeding competition. Three predictions were made based on this suggestion: 1. Cygnets should remain closer to parents in more crowded flocks; 2. Cygnets should remain closer to parents when feeding on foods that produce aggressive encounters (eg: agricultural crops); 3. Cygnets of smaller body size and females will remain closer to parents.

(Source: Arpingstone; in public domain)

Figure 3.1 - Bewick's swans. Observations were made using point or focal sampling: "a sampling rota was developed in which, before each feed, five focal individuals were watched, each for 1 min every 10 min, such that A was watched for 1 min, Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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then after a gap of 1 min, B was watched for 1 min and so on for C, D, and E and then A was found again" (p940). During that sample minute, all aspects of the birds interactions were recorded including distance to mate, cygnet, or parents; and distance to three nearest unrelated neighbours. Event sampling was used for aggressive encounters (table 3.5). POINT OR FOCAL SAMPLING

EVENT SAMPLING

Description

Record what individual is doing at point in time

Record details of an event every time it occurs

Advantage

Record for all individuals being observed

Records key event as often as it happens

Disadvantage

May miss information because focused on one individual at a time

Tends to look at the event out of context of other behaviour

Table 3.5 - Point and event sampling in observations. Cygnets were significantly more successful in aggressive encounters when near parents (within 4 swan lengths) than alone (75% vs 33% won; X² = 4.2; df = 1; p<0.05). Concerning the three predictions above: 1. Cygnets remained nearer to parents in more dense flocks (average 1.5m away vs 2.3m in less dense flocks). 2. When the flock was eating waste potatoes that produced more aggression, the cygnets remained approximately half as near to parents compared to feeding on winter wheat where less aggression occurred. Mean relative distance of cygnet to parent was 1.0 for wheat and 0.6 for potatoes (p<0.05). 3. Females and smaller cygnets remained closer to parents. The cygnets were more confident closer to parents as shown by amount of time feeding: over 80% for those in close proximity compared to less than 40% when cygnet was seven or more swan lengths away. PPC meant that parents intervened in aggressive encounters on behalf of their cygnets (34% of encounters), and the presence of parents was enough in some cases to step aggression developing, especially with subordinate birds. But intervention had a cost for the parents, if only to stop them feeding. For example, during OctoberNovember, parents spent under 60% of time feeding Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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compared to 80% for adult pairs without cygnets. The proximity changed over the winter period, however, and it was reduced by January-February (mean relative distance of 1.27 vs 0.72 in November-December). As the cygnets moved further away, the parents spent more time feeding (80% of time in February-March). There were other beneficial changes in parents' behaviour over the winter (table 3.6). PARENTS

PAIRS WITHOUT CYGNETS

SIG

Mean percentage of observations when adults alert (ie: heads up in vigilant position): Oct-Nov Dec-March

40 20

20 25

<0.05 ns

Threat frequency (per min) during feeding: Oct-Nov Dec-Feb

2.4 2.0

1.2 1.2

<0.02 ns

Table 3.6 - Changes in two behaviours of parents over the winter. Any direct costs to parents, like reduced feeding, while involved in PPC is compensated by "indirect fitness" in the survival of the offspring through feeding or protection from aggression by unrelated adults. Table 3.7 summarises the main advantages and disadvantages of PPC.

ADVANTAGES

DISADVANTAGES

1. Indirect fitness with a greater chance of the offspring's survival and their production of offspring.

1. Cost to parents in terms of less opportunity for feeding.

2. To teach offspring key survival skills like food sources and migration. 3. To protect offspring from predators and aggressive conspecifics (feeding competition). 4. The offspring benefit in terms of protection and feeding.

2. Cost to parents in terms of less opportunity for mating and further offspring. 3. Risk to parents in protecting offspring. 4. Offspring may not be able to fend for themselves when PPC ends. 5. Offspring that need PPC can be highly vulnerable in the first few days, weeks, and months.

5. PPC means that offspring can still developed after birth/hatching.

Table 3.7 - Main advantages and disadvantages of PPC. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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3.3. RED DEER AND SEX OF OFFSPRING Parental investment in their young may vary depending on the sex of the offspring. For example, female red deer (Cervus elaphus) invest more in individual sons than individual daughters (Clutton-Brock et al 1981). This is shown in the red deer on the Scottish island of Rhum - male calves have significantly longer gestation lengths (236.1 vs 234.2 days for females), significantly heavier birth weight (6.72 vs 6.23kg), and suck from their mothers significantly more frequently (5.1 vs 2.6 daily suckling bouts). Also hinds who reared male calves were less likely to produce a calf the following breeding season, and those that did, gave birth later in the season compared to mothers of female calves (CluttonBrock et al 1981). Observations over twenty years on Rhum show a clear pattern between "maternal rank" and the production of male offspring. Maternal rank is defined as "the ratio of animals which the subject threatened or displaced to animals which threatened or displaced it weighted by the identity of the animals displaced" (Clutton-Brock and Godfray 1991) (table 3.8). MATERNAL RANK low

high

0.1 0.3 0.5 0.8 1.0

APPROXIMATE PERCENTAGE OF OFFSPRING BORN MALE 20 30 45 65 75

(After Clutton-Brock et al 1986)

Table 3.8 - Correlation between "maternal rank" and percentage of male offspring born. The sex of the offspring in polygynous mammals is influenced by maternal conditions. Mothers in good conditions produce sons and those in poor conditions produce daughters. This is known as the Trivers-Willard hypothesis (Trivers and Willard 1973). The maternal conditions will be linked to the resources available to survive and raise the offspring. Where resources are plentiful, then the maximum genes can be passed into future generations by male offspring based on grandchildren (figure 3.2). Daughters will always find a mate even if this limits the number of grandchildren. The production of daughters is a better strategy where Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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resources are limited.

↓

GOOD MATERNAL CONDITIONS

POOR MATERNAL CONDITIONS

MOTHER ↓

MOTHER ↓

MANY OFFSPRING ↓

ONE OFFSPRING ↓

SONS BETTER STRATEGY ↓ ↓

DAUGHTERS - ALWAYS FIND MATE ↓ GRANDCHILD GUARANTEED

FEMALE ↓

FEMALE ↓

FEMALE ↓

MANY GRANDCHILDREN FOR MOTHER = MORE GENES INTO FUTURE

DAUGHTERS GUARANTEED MATE, BUT LIMITED GRANDCHILDREN

BUT SONS = RISK OF MANY MATINGS VS MAY NOT MATE

Figure 3.2 - Different strategies for offspring in different maternal conditions. The dominance of the female will also influence the success of the offspring. High-ranking hinds produce more sons because of the greater lifetime reproductive success for those sons, and low-ranking hinds produce more daughters (Cockburn 1999). Work by Kruuk et al (1999) on Rhum island has noted that with increasing population density, high-ranking females produce more daughters. Increasing population density is an example of poor maternal conditions, and thus the production of daughters is a better evolutionary strategy. However, Cockburn (1999) argues that male foetuses are more sensitive to resource availability, and more of them may be dying before birth with the increasing population density. The increase in female births is in fact the increased survival of females at birth. It is unclear how the process of "choosing" the sex of the offspring works. For example, the hormones from the mother could influence the production of girls, and testosterone from the fathers for boys. High social ranking males could have more testosterone and thus "determine" the sex of the offspring as male (Cartwright 2000). Maybe high-ranking hinds have more testosterone as well, and this explains the situation in red deer.

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3.4. REFERENCES Breder, C & Rosen, D (1966) Modes of Reproduction in Fishes Natural History Press Cartwright, J (2000) Evolution and Human Behaviour Macmillan

New York:

Basingstoke:

Clutton-Brock, T.H & Godfray, C (1991) Parental investment. In Krebs, J.R & Davies, N.B (eds) Behavioural Ecology: An Evolutionary Approach (3rd ed) Oxford: Blackwell Science Clutton-Brock, T.H et al (1981) Parental investment in male and female offspring in polygynous mammals Nature 289, 487-489 Clutton-Brock, T.H et al (1986) Great expectations: Dominance, breeding success and offspring sex ratios in red deer Animal Behaviour 460-471 Cockburn, A (1999) Deer destiny determined by density Nature 407-408

34,

399,

Kruuk, L.E.B et al (1999) Population density affects sex ratio variation in red deer Nature 399, 459-461 Maynard Smith, J (1977) Parental investment - a prospective analysis Animal Behaviour 25, 1-9 Maynard Smith, J (1978) The ecology of sex. In Krebs, J & Davies, N (eds) Behavioural Ecology: An Evolutionary Approach Oxford: Blackwell Scott, D.K (1980) Functional aspects of prolonged parental care in Bewick's swans Animal Behaviour 28, 938-952 Trivers, R (1972) Parent-offspring conflict American Zoologist 249-264

14,

Trivers, R & Willard, D (1973) Natural selection of parental ability to vary the sex ratio of offspring Science 179, 90-92

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4. ADVANTAGES AND DISADVANTAGES OF LEK MATING 4.1. Introduction 4.2. Examples of lek behaviour 4.3. References 4.1. INTRODUCTION Lek polygyny is a specific type of polygamy where males mate with multiple females. The male sets up a "symbolic territory" (a territory with little or no resources) in which to advertise himself in an area near to other leks, and females check out the options before mating with the best male. Good quality males get to mate with many females, and females can mate only with the best male (table 4.1). Parental care is solely the concern of females in such species. ADVANTAGES

DISADVANTAGES

1. Convenient for females to assess all the males in one place and choose the best quality.

1. The system is open to exploitation by poor quality males who lurk near the best quality males and attempt forcible copulation.

2. Works well in normally geographically dispersed species that come together at the breeding season only. 3. Good quality males get to mate with many females. 4. No costs to males of maintaining territory for long periods of time. 5. Females can mate in lek without being harassed by other males.

2. Best quality males may run out of sperm for late-arriving females. 3. Risk of interference from males in neighbouring leks. 4. Problem of best quality males being temporarily monopolised by other females. 5. Females do not know if males with leks near centre are "honest signals" of good quality.

Table 4.1 - Main advantages and disadvantages of lekking. When males establish their mating territory, resources are generally not important as in a "normal" territory which is defended because of its resources. The choice of a lekking site seems to be visibility to females; eg: Uganda kob (Kobus kob thomasi) choose areas with little vegetation (Wikelski et al 1996).

4.2. EXAMPLES OF LEK BEHAVIOUR Wikelski et al (1996) studied the marine iguanas Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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(Amblyrhynchus cristatus) on Genovesa island (Galápagos archipelago, Ecuador). The mating season lasts from early December to early January, and three seasons were studied. Individual animals were marked by hot branding which left an identifiable mark while causing only superficial skin damage. Four observers were trained for three days to aid inter-observer reliability. Observation took place during daylight hours by following a fixed route along the beach area. Focal (or point) observations were made at four locations, and all copulations were recorded (behaviour sampling) 6. Three types of males were observed:


Territorial males who occupied and defended a particular mating area for five consecutive days. They were larger than the other types of males. Females preferred to mate in territories because it avoided harassment from other males;




Marginal males who did not occupy a territory and moved around attempting to forcefully mate with any females they mate;




Sneaker males who were the size of females (smaller than the average male) and who attempted to mate in territories where the territorial male was absent.

Females, who copulated only once per breeding season, preferred to mate with territorial males (table 4.2), and with larger ones. Small territorial males were more successful if based close to large territorial males. Beehler and Foster (1988) called this the "hotspot phenomena" - small territorial males get "accidental matings" when near large territorial males. TERRITORIAL MALES

MARGINAL MALES

SNEAKER MALES

Body mass (g)

657

503

424

Total copulations observed

129

6

6

Copulations per male

3.1*

0.4

0.3

(* = significantly different to other two; p = 0.01) (After Wikelski et al 1996)

Table 4.2 - Mating success of different types of male iguanas in the 1992-3 breeding season.

6

Focal or point sampling records what is happening at a particular moment in time, while behaviour sampling records every occasion of a particular behaviour. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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A lek is like a "male beauty contest" for the females. Comparison is possible to aid the choice of males. What are the characteristics of males that improve their mating success in this "beauty contest"? Many studies have looked at individual species using "vote counting" (ie: number of matings) as success. Fiske et al (1998) sought to establish the general patterns of male mating success in leks using a "bare-bones" meta-analysis (Hunter and Schnidt 1990) of forty-eight studies. Table 4.3 summarises the characteristics analysed. CHARACTERISTICS

CONCLUSIONS (= mating success)

Attendance - time spent on lek

Positive correlation: more time

Display frequency; eg: amount of time spent calling

Positive correlation: more time

Fighting frequency

Positive correlation: more fighting

Location of territory

Negative correlation: nearer lek centre

Size of territory

No correlation

Male body size

Weak positive correlation: larger body

Extravagant morphological traits; eg: antlers

Positive correlation: larger

Male age

Positive correlation: older

Table 4.3 - Characteristics of males that gain mating success in leks. Meta-analysis (Glass 1977) allows the "quantitative summary of statistical tests from multiple studies" (Fiske et al 1998) by standardising the data (through the effect size), and making general conclusions. However, there are limitations to this technique (Fiske et al 1998): i) Sample size of studies to use can be small; eg: nine studies on fighting frequency, and seven on age. ii) Dependent upon the studies performed. For example, fourteen of 27 species studied were birds, eight were amphibians, 2 were insects, and three mammals. iii) The "file drawer" problem. Significant results tend to get published, so it is not known how many nonsignificant studies were performed and not published. Thus published studies may be unrepresentative of all the studies performed. Statistical techniques have been developed to overcome this problem (eg: number of studies needed to change effect size; Rosenthal 1979). Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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iv) "Apples and oranges". This is the problem that meta-analysis combines studies that were measuring different things and in different ways. Female choice of mate depends upon "honest signals" of the male's quality. The usual signals are body size and plumage. One signal specific to lekking is the position of the territory towards the lek centre. Territories at the lek centre should belong to highranking males and/or those who are superior in ability to maintain such a territory if the signal is honest. The signal will not be honest if there is "queue-jumping". This is where fighting occurs, for example, and a lowerranked individual gains a higher rank by winning. Kokko et al (1998) investigated lek positions among black grouse (Tetrao tetrix)(figure 4.1) at sites in central Finland over a eight-year period. The males at the centres tended to be superior in terms of fighting and survival abilities. Queue-jumping tended not to happen often because of the risks of injury from fights. The males queued for central lek territory (ie: waited until high-ranking males leave). It is an "evolutionary stable strategy" (Maynard Smith 1982) - the best strategy in terms of costs and benefits.

(Source: Gagea; in public domain)

Figure 4.1 - Black grouse in Sweden. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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It is generally assumed that females will mate only once with the best quality male, but this is not always the case as with, for example, the ruff (Philomachus pugnax). This shorebird has a genetic dimorphism in males; ie: two different males. One type has darker plumage and defends a "mating court" (1m²) during the lekking season. The other is lighter and hangs around the mating courts ("satellite behaviour")(Lank et al 2002). Lank et al (2002) studied the mating behaviour of female ruffs (called "reeves") on a shoreline in Finland. About a quarter were observed to mate with more than one male on a single visit to the lek, and 17 of thirty-four broods had multiple fathers. Fourteen out of 23 reeves observed mated with both types of males. Why do reeves mate with multiple males? The simple answer is to diversify the genetics of the offspring. The costs for females of multiple matings are low because they do not risk the loss of paternal care as male support does not occur. "For whatever reason, a female’s mating rule in many lekking species may be not the oftstated search for the highest quality male, but rather to seek several high quality mates" (Lank et al 2002 p214). 4.3. REFERENCES Beehler, B.M & Foster, M.S (1988) Hotspots, hotspots and female preference in the organisation of lek mating strategies American Naturalist 131, 203-219 Fiske, P et al (1998) Mating success in lekking males: A meta-analysis Behavioural Ecology 9, 4, 328-338 Glass, G.V (1977) Integrating findings: The meta-analysis of research Review of Research in Education 5, 351-379 Hunter, J.E & Schmidt, F.L (1990) Methods of Meta-Analysis: Correcting Error and Bias in Research Findings Newbury Park, CA: Sage Kokko, H et al (1998) Queuing for territory positions in the lekking black grouse (Tetrao tetrix) Behavioural Ecology 9, 4, 376-385 Lank, D.B et al (2002) High frequency of polyandry in a lek mating system Behavioural Ecology 13, 2, 209-215 Maynard Smith, J (1982) Evolution and the Theory of Games Cambridge University Press

Cambridge:

Rosenthal, R (1979) The "file-drawer problem" and tolerance for null results Psychological Bulletin 86, 638-641 Wikelski, M et al (1996) Lekking in marine iguanas: Female grouping and male reproductive strategies Animal Behaviour 52, 581-596

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5. ADVANTAGES AND DISADVANTAGES OF NONREPRODUCTIVE SEX IN ANIMALS 5.1. Post-conception mating 5.2. Homosexual interactions 5.3. References 5.1. POST-CONCEPTION MATING Sex is about reproduction among animals. Yet nonreproductive sex exists, for example, by pregnant or lactating females. What are the reasons for such behaviour, particularly among females (also known as post-conception mating)? Table 5.1 lists the advantages and disadvantages for males and females.

MALES

FEMALES

ADVANTAGES

DISADVANTAGES

1. Pleasure.

1. Waste of sperm and cost of replenishing supply.

2. Strengthens the bond in monogamous species.

2. Energy costs of sex.

3. Male sexual competition.

3. Risks of sexually transmitted disease.

1. To gain favour with dominant males.

1. Risks of injury during sex.

2. To gain protection for self and offspring from dominant males. 3. To confuse males about paternity and gain support, and/or avoid infanticide.

2. Risks of sexually transmitted disease. 3. Does not confuse male about paternity if he knows that sex non-reproductive (eg: female shows signs of pregnancy). 4. Energy costs of sex.

4. Female sexual competition by reducing sperm of male available to other females. 5. Pleasure. 6. Strengthens the bond in monogamous species.

Table 5.1 - Advantages and disadvantages of nonreproductive sex. Stoinski et al (2009) observed one male gorilla with four females at the Zoo Atlanta in the USA. The group of five western lowland gorillas (Gorilla gorilla gorilla)(figure 5.1) were observed for a total of 273 Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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hours over 245 days between December 2004 and December 2006. Females encouraging sex (solicitation) was defined as "slowly approaching male with direct eye contact, often accompanied by pursued lips and attempts to touch the male" (p588).

(Source: Arpingstone; in public domain)

Figure 5.1 - Male gorilla. Non-reproductive females offered sex when other females were sexually active (table 5.2). TOTAL SOLICITATIONS

KUCHI

KUDZOO

SUKARI

LULU

Single occurrence days - only one female sexually active

36

17

6

3

10

Co-occurrence days - another female sexually active

75

20

9

17

29

Significance

<0.05

ns

<0.05

<0.01

<0.01

(After Stoinski et al 2009)

Table 5.2 - Solicitations by four female gorillas. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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It seemed to be a case of if they are doing it, I better do it too. For the non-reproductive females, offering sex could have been to gain favour and protection of the self and offspring from the male, or to stop the male copulating with the reproductive females by depleting his sperm. When there is more than one male, non-reproductive sex by the female is a way of confusing the male about paternity, and thereby encouraging him to care for her and her offspring. 5.2. HOMOSEXUAL INTERACTIONS A different aspect to non-reproductive sex is where same-sex individuals court and attempt to mate "homosexual interactions" (Maklakov and Bonduriansky 2009). Such behaviour may assert dominance over rivals, or be practice for heterosexual encounters. More generally, it is felt to be a perceptual error (or lack of sex recognition). For example, male water bugs (Palmacorixa nana) mount any individual large than themselves because females are generally larger than males (Aiken 1981). Maklakov and Bonduriansky (2009) investigated homosexual interactions in two species of insects:


Carrion fly (Prochyliza xanthostoma) - Males fight over territories from which females are courted with a "dance". The cost of homosexual interactions are energy loss through the "dance" and injury during fights;




Seed beetle (Callosobruchus maculatus) - Males chase females and mount without courtship. Sex is dangerous for females as the penis has spines attached. The cost of homosexual interactions would be loss of energy and water, and fatal injury as the mounting male's genitalia can get stuck under the elytra (hardened forewings) of another male.

The cost of homosexual interactions were measured in terms of deaths in six experimental conditions - males and females alone, all male and all female groups, and males and females in mixed sex groups. In both species, males in all male groups had shorter lifespans. In terms of evolution, male homosexual mounting in insects is the product of the benefits of rapid, indiscriminate mating over the costs of discriminating males from females (Thornhill and Alcock 1983). As long as the former is greater, then there is no need for the evolution of mechanisms to identify same sex. Animal Behaviour: Advantages and Disadvantages No.2; Kevin Brewer; 2009 ISBN: 978-1-904542-47-6

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5.3. REFERENCES Aiken, R.B (1981) The relationship between body-weight and homosexual mounting in Palmacorixa nana Walley (Heteroptera: Corixidae) Florida Entomologist 64, 267-271 Maklakov, A.M & Bonduriansky, R (2009) Sex differences in survival costs of homosexual and heterosexual interactions: Evidence from a fly and a beetle Animal Behaviour 77, 6, 1375-1379 Stoinski, T.S et al (2009) Sexual behaviour in female western lowland gorillas (Gorilla gorilla gorilla): Evidence for sexual competition American Journal of Primatology 71, 7, 587-593 Thornhill, R & Alcock, J (1983) The Evolution of Insect Mating Systems Cambridge, MA: Harvard University Press

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