Research Essay

Russell 1 Riley Russell Prof. Kretzer English 1201.920 13 April 2019

The Evolution of Extra-pair Paternity of Birds When you think of birds, you might think of the idea of perfect monogamy seemingly exemplified by them. However, as said by Josh Gabbatiss, a writer for BBC Earth, "bird love lives contain more drama than your average soap opera" (21). This is because the majority of bird species engage in extra-pair paternity (Akçay and Roughgarden 855), or creating offspring with an individual other than one's social mate. Why this might occur is a controversial topic in avian biology. The reasons for males to engage in it are understood, as they can easily increase the number of offspring they father with little consequence, but females often solicit (and, according to Petrie and Kempenaers, control the success of [52]) extra-pair copulations, even though it does not increase the number of young produced and could result in negative effects (such as punishment or aggression by the female's social mate). The explanations for this perplexing behavior are numerous; in the past, they have focused on the idea that extra-pair paternity is beneficial to females (or their offspring), whereas more diverse hypotheses have emerged recently (Forstmeier ​et al.​, "Female Extra-pair Mating" 456). This research paper will explain why these newer hypotheses are more promising in their explanatory power of extra-pair paternity compared to older ones like the genetic benefits hypothesis, which are not supported by

Russell 2 empirical evidence. Additionally, it will argue that different hypotheses are more applicable to certain species, primarily because of the preconditions required by some explanations. Due to the large number of hypotheses proposed, this paper will focus on only four explanations for extra-pair paternity: the genetic benefits hypothesis, the fertility insurance hypothesis, the context-dependent genetic benefits hypothesis, and the genetic constraints hypothesis. The genetic benefits hypothesis proposes that extra-pair offspring have increased fitness (in biology, this refers to how well an organism can survive and reproduce). There are two variants of this: the good genes hypothesis, which claims that a fitness benefit occurs due to certain males having more universally "attractive" qualities, and the genetic compatibility hypothesis, which suggests that extra-pair fathers are selected based on how well their genes combine with the mother (this is often measured by seeing how related the mother and father are; the more related, the less compatible; Akçay and Roughgarden 856-857). The next hypothesis is the fertility insurance hypothesis, which says that females engage in extra-pair paternity to reduce the number of infertile eggs they have (Forstmeier ​et al.​, "Female Extra-pair Mating" 458). A more recent explanation for extra-pair paternity is the context-dependent genetic benefits hypothesis, which, similar to the first explanation, posits that extra-pair offspring experience genetic benefits; however, these advantages can only be seen in certain environments (Hallinger 2). Another recent hypothesis, the genetic constraints hypothesis, states that extra-pair paternity evolved because it is correlated with positive fitness benefits elsewhere. This explains how the behavior could evolve even if it is maladaptive (detrimental), as some studies have found. There are two variants of this: the intersexual antagonistic pleiotropy hypothesis and the intrasexual antagonistic pleiotropy hypothesis. The first claims that extra-pair paternity evolved because

Russell 3 genes affecting male fitness also modulate extra-pair mating behavior in females. In this scenario, even if a female's fitness is lowered because of extra-pair copulations, the benefits to males would more than offset the consequences endured by the female, resulting in the evolution of extra-pair paternity. The latter variant says that extra-pair paternity occurs because genes important in ensuring a female's fitness, like the receptivity to her within-pair mate, also control extra-pair paternity. As in the first variant, the selective pressure on other genes (in this case, those of the female) overcomes the pressure against extra-pair paternity, resulting in its evolution (Forstmeier ​et al​., "Female Extra-pair Mating" 460-461). The genetic benefits hypothesis is arguably the best studied explanation for extra-pair paternity. Important tests of it include: whether extra-pair mates differ from within-pair mates in terms of genetic quality or in relatedness to the females, whether extra-pair offspring survive better than within-pair offspring, and (for the genetic compatibility variant) whether the relatedness of a pair is correlated with the occurrence of extra-pair paternity (Akçay and Roughgarden 856). In a 2007 analysis conducted by Akçay and Roughgarden, faculty members at Stanford University, it was found that just under half of the studies analyzed supported the genetic benefits hypothesis (42% supported the good genes hypothesis, and 44% supported the genetic compatibility hypothesis), and only six out of twenty-three studies found non-contradictory significant differences between extra- and within-pair offspring (858-859). The authors then conducted a meta-analysis on the studies, finding (after accounting for publication bias) that only the size and age of extra-pair sires were significantly different from within-pair males; importantly, offspring survival was not found to be significantly positively related to extra-pair status, whether or not publication bias was considered (862). This shows that

Russell 4 extra-pair status likely does not confer a fitness benefit to a female's offspring, at least in the first year of their life. In addition, studies such as the third chapter of Hallinger's 2017 thesis often find that extra-pair offspring do not have better future reproductive success than within-pair young (65). Adding to this lack of fitness benefit for extra-pair offspring is that extra-pair males usually do not differ in the features predicted by either version of the genetic benefits hypothesis. Contrary to the predictions of the good genes hypothesis, extra-pair mates do not have significantly different secondary sexual traits (traits that appear at sexual maturity; breasts are an example of this in humans), although they do generally differ in size and age (Akçay and Roughgarden 862). Furthermore, according to a recent meta-analysis by Arct ​et al.​ , researchers at Jagiellonian University, a prediction of the genetic compatibility hypothesis, that females more closely related to their within-pair mate will have more extra-pair offspring, was only significantly supported when microsatellite markers (repeating segments of DNA that vary widely between individuals) were used to determine paternity and the relatedness of the within-pair male to the female (962). However, as mentioned by Wetzel and Westneat, faculty members at the University of Kentucky, using microsatellite markers in this way can produce results biased towards confirming the genetic compatibility hypothesis. This is because studies are more likely to detect extra-pair paternity if the within-pair male and female are more closely related, meaning that extra-pair fathers will generally appear to be less related to the female (2011-2012). Thus, the results obtained by Arct ​et al​. are likely invalidated by the methodological problems present. This all suggests that the genetic benefits hypothesis is a very unlikely explanation for the occurrence of extra-pair paternity in birds; as mentioned before,

Russell 5 there seems to be no fitness benefit that extra-pair offspring enjoy, so females do not increase the fitness of their offspring (and therefore themselves) by engaging in extra-pair paternity. Because of the failure of the genetic benefits hypothesis, some researchers started to turn towards the fertility insurance hypothesis. This hypothesis is likely to be flawed, however, as the benefits of mating with more mates to increase fertility may be offset by the increased chance of pathological polyspermy (where more than one sperm fertilize an egg) that increased sperm numbers may bring. Pathological polyspermy is detrimental as it can result in an abnormal number of chromosomes if more than one sperm eventually fuse with the nucleus of the egg; this is likely to be fatal to the resulting young. Increased amounts of sperm would occur because there would be more males to provide sperm in larger numbers (due to both sperm competition, where males ejaculate increased amounts of sperm in an attempt to ensure paternity, and the larger on average number of sperm that are ejaculated from extra-pair copulations; Forstmeier ​et al​., "Female Extra-pair Mating" 457-458). Empirical evidence has also failed to support the explanation: the hypothesis predicts that species with higher infertility rates should have higher levels of extra-pair paternity, but this was not met in a meta-analysis conducted by Morrow ​et al​., who are researchers at Uppsala University and the University of Toronto, in 2002 (702). Additionally, the prediction that an infertile social mate should increase rates of extra-pair paternity was not seen in a study on zebra finches: swapping eggs to make certain pairs appear more fertile and others less did not change individual rates of extra-pair paternity according to a 2012 study by Ihle ​et al.​ , faculty members at the Max Planck Institute for Ornithology (119). Another earlier study by Birkhead and Fletcher, researchers at the University of Sheffield, found similar results for vasectomized male zebra finches: females mated to these males did not have

Russell 6 increased rates of extra-pair copulations, despite the fact that their social mate could not fertilize an egg (329). These studies show a clear rejection of the idea that defending against infertility drives the species-wide evolution of extra-pair paternity; even in some species with very high rates of fertility (and thus virtually no need to ensure fertility by mating with other males), extra-pair paternity can still be seen. However, the hypothesis that individuals may engage in extra-pair paternity when their social mate is infertile cannot be discarded for all species, although it can be firmly rejected for the zebra finch, as infertile mates did not spur females into increased extra-pair paternity. This may be because zebra finches form strong pair bonds that last for multiple breeding attempts; the selective pressure resulting in the evolution of this likely overcame the pressure that would have resulted in decreased female fidelity due to male infertility (Ihle ​et al​. 124-125). In other species, with more ephemeral ties, extra-pair paternity might have evolved partially due to male infertility. Additionally, in birds like the bluethroat, where infertility often takes the form of a complete lack of sperm, fertility insurance may be at work; this is because fertile sperm will take precedence over no sperm, unlike in situations where there is no preference for fertile sperm versus infertile sperm. This is empirically supported by the occurrence of some clutches (sets of eggs) which are composed completely of extra-pair offspring (Ihle ​et al.​ 119). This underscores the potential for extra-pair paternity to have evolved for different reasons in different species. The wide variation in results of tests for the genetic benefits hypothesis has led some researchers to investigate the context-dependent genetic benefits hypothesis. In this case, positive, neutral, and negative results would be expected when tests of the genetic benefits hypothesis are conducted, as differences in the environment would change how extra-pair

Russell 7 paternity modulates offspring fitness. According to Schmoll, a faculty member of the University of Bielefeld, studies on this hypothesis have found support for the idea that extra- and within-pair offspring do better in different environments (S270). For example, a study on the coal tit found that extra-pair offspring (compared to within-pair offspring from the same broods) were more likely to be found in the population the year after they hatched when they came from broods later in the season, but not when they came from earlier broods (Schmoll S270). In a study on tree swallows performed by Hallinger for her PhD thesis, it was found that extra-pair offspring exposed to mounts of predators were generally larger than within-pair offspring subjected to the same treatment, whereas within-pair offspring were often larger than extra-pair offspring when mounts of non-predators were shown (13). This shows how benefits are only seen in certain circumstances. It was also found that extra- and within-pair offspring did not differ in lifetime fitness, but under some conditions, within-pair offspring outperformed extra-pair offspring. Specifically, they produced more fledglings (birds that have just acquired the feathers they need to fly) when they experienced more variable temperatures while being incubated, less variable temperatures during their first few days after hatching, less variable temperatures just before fledging, and warmer temperatures just before fledging. These more successful within-pair offspring also produced more fledglings than within-pair offspring that were not subject to these conditions (Hallinger 65-66). Therefore, extra-pair offspring may sometimes have decreased fitness compared to within-pair offspring, accounting for studies that have found extra-pair paternity to be detrimental to the fitness of a female's young. This hypothesis also gives insight on how different pressures likely drive extra-pair paternity, as can be seen in the debate on whether good environmental conditions reveal or conceal benefits. Overall, the

Russell 8 context-dependent genetic benefits hypothesis is very promising, although more investigation is needed to confirm it. This explanation may also act in concert with others for a full understand of extra-pair paternity. Some authors have turned to the genetic constraint hypothesis, which explains why females might engage in extra-pair paternity even if it is detrimental to them. Apart from one study, little empirical research has been done on this topic. In this study, conducted by Forstmeier ​et al​., faculty members at the Max Planck Institute for Ornithology, it was found that in closely related zebra finches there is a strong correlation between male courtship rate and both female rates of extra-pair paternity and female extra-pair response (this is a measurement of how a female responds to extra-pair males courting her), providing support for the intersexual antagonistic pleiotropy hypothesis. There was not a strong correlation between traits such as female extra-pair paternity and how females responded to courtship when they were not paired with a social mate ("Female Extrapair Mating Behavior" 10609), indicating that female receptivity to potential mates does not correlate with extra-pair paternity, and therefore that this behavior would not evolve for the reasons predicted by the intrasexual antagonistic pleiotropy hypothesis. These results might be explained by the strength of the zebra finch's pair bond: this bond likely evolved at the same time in both sexes, so mating behavior probably is similar between them, allowing something beneficial to only one sex to be seen in both. This idea is reinforced by the similar courtship behaviors of male and female zebra finches (Forstmeier ​et al.​ , "Female Extrapair Mating Behavior" 10610).

Russell 9

Fig. 1. Graph of correlations between personality traits and extra-pair copulations in humans. This supports the intersexual antagonistic pleiotropy hypothesis as it shows that extra-pair mating behavior in males and females is correlated with the same behavioral traits, which may result from the same genes. This may also be the case in birds (Forstmeier ​et al.​ , "Female Extra-pair Mating" 460-461). As mentioned previously, stronger pair bonds and similar courtship behaviors between the sexes can lead to the evolution of extra-pair paternity as predicted by the intersexual antagonistic pleiotropy hypothesis. A weaker pair bond may also lead to the evolution of extra-pair paternity, but instead along the lines anticipated by the intrasexual antagonistic pleiotropy hypothesis. This is because females that can mate with males they are less familiar with would have an advantage when divorce is common (as would be expected when the pair

Russell 10 bond is weaker); this proclivity would lead to increased rates of extra-pair paternity (Forstmeier et al.​ , "Female Extra-pair Mating" 461-462). In a few species, like the red-winged blackbird, access to food in adjacent territories and defense by males can explain the evolution of female-driven extra-pair paternity. According to the results of an experiment conducted by Gray, a faculty member of the University of Washington, female red-winged blackbirds were allowed to feed on the territory of males that they had engaged in extra-pair copulations with; normally, the male would defend its territory from individuals outside of the pair bond. Additionally, these males were more aggressive to mock predators in adjacent territories occupied by a female they had copulated with (625). Extra-pair paternity may also be a mechanism to avoid infanticide by unrelated males. However, this idea is mostly based on circumstantial evidence from non-avian taxa. But, in birds like the tree swallow, where infanticide has only been observed to occur after egg-laying is complete (likely because a new male can copulate with the female and fertilize at least one egg), extra-pair paternity may dissuade new males from killing the young (Forstmeier ​et al.​ , "Female Extra-pair Mating" 459). These examples show how extra-pair paternity can evolve due to species-specific circumstances. Active female participation in extra-pair paternity is a confusing aspect of avian behavior. This lack of understanding is not mitigated by the fact that some high-profile studies support older hypotheses (Akçay and Roughgarden 866), like the genetic benefits hypothesis, that have been rejected after years of research and evidence. In the certain cases, like that of the genetic compatibility hypothesis, the only support comes from methodologically flawed data. However, recent ideas, like the context-dependent genetic benefits hypothesis and the genetic constraint

Russell 11 hypothesis, are very promising in the extent that they can explain female-driven extra-pair paternity. The context-dependent genetic benefits hypothesis, for example, is supported by multiple studies, and has the power to explain the wide variety of results that tests of the genetic benefits hypothesis have yielded. It is important to note that some explanations only apply to certain species. For example, the application of the variants of the genetic constraint hypothesis likely depends on the strength of the pair bond in the species being studied. Finally, more recent explanations for extra-pair paternity should not be immediately accepted; because of the lack of attention given to them, they still need more empirical support.

Russell 12 Works Cited Akçay, Erol, and Joan Roughgarden. "Extra-pair Paternity in Birds: Review of the Genetic Benefits." ​Evolutionary Ecology Research,​ vol. 9, no. 5, 2007, pp. 855-868. Arct, Aneta, ​et al.​ "Genetic Similarity Between Mates Predicts Extrapair Paternity—a Meta-analysis of Bird Studies." ​Behavioral Ecology,​ vol. 26, no. 4, 2015, pp. 959-968. OhioLINK Electronic Journal Center,​ doi:10.1093/BEHECO/ARV004. Birkhead, Timothy Robert, and F. Fletcher. "Male Phenotype and Ejaculate Quality in the Zebra Finch ​Taeniopygia guttata​." ​Proceedings of the Royal Society B,​ vol. 262, no. 1365, 1995, pp. 329-334. Forstmeier, Wolfgang, ​et al.​ "Female Extra-pair Mating: Adaptation or Genetic Constraint?" Trends in Ecology & Evolution,​ vol. 29, no. 8, 2014, pp. 456-464. ​OhioLINK Electronic Journal Center​, doi:10.1016/J.TREE.2014.05.005. Forstmeier, Wolfgang, ​et al.​ "Female Extrapair Mating Behavior Can Evolve Via Indirect Selection on Males." ​PNAS​, vol. 108, no. 26, 28 June 2011, www.pnas.org/content/108/26/10608.full. Accessed 22 Mar. 2019. Gabbatiss, Josh. "Why Pairing Up for Life is Hardly Ever a Good Idea." ​BBC Earth​, 13 Feb. 2016, www.bbc.com/earth/story/20160213-why-pairing-up-for-life-is-hardly-ever-a-good-idea? scrlybrkr. Accessed 13 Apr. 2019. Gray, Elizabeth M. "Female Red-winged Blackbirds Accrue Material Benefits from Copulation with Extra-pair Males." ​Animal Behaviour,​ vol. 53, no. 3, 1997, pp. 625-639.

Russell 13 Hallinger, Kelly Kristen. ​Context Dependent Fitness Consequences of Extra-pair Paternity in Tree Swallows (T ​ achycineta bicolor​).​ PhD Thesis, Cornell University, 2017. Ihle, Malika, ​et al.​ "Does Hatching Failure Breed Infidelity?" ​Behavioral Ecology​, vol. 24, no. 1, 2013, pp. 119-127. Morrow, E. H., ​et al​. "The Evolution of Infertility: Does Hatching Rate in Birds Coevolve with Female Polyandry?" ​Journal of Evolutionary Biology​, vol. 15, no. 5, 2002, pp. 702-709. Petrie, Marion, and Bart Kempenaers. "Extra-pair Paternity in Birds: Explaining Variation Between Species and Populations." ​Trends in Ecology and Evolution​, vol. 13, no. 2, 1998, pp. 52-58. Schmoll, Tim. "A Review and Perspective on Context-dependent Genetic Effects of Extra-pair Mating in Birds." ​Journal of Ornithology,​ vol. 152, supplement 1, Sept. 2011, pp. 265-277. Wetzel, Daniel P., and David F. Westneat. "Heterozygosity and Extra-pair Paternity: Biased Tests Result from the Use of Shared Markers." ​Molecular Ecology,​ vol. 18, no. 9, May 2009, pp. 2010-2021.