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Mate choice and the evolution of female promiscuity in a socially monogamous species
Mate choice and the evolution of female promiscuity in a socially monogamous species
Chapter 1: Male zebra fiches have limited ability to identify high-fecundity females Abstract: In species with bi-parental care and lifetime monogamy, the fecundity of a male’s partner can be a major component of his fitness, but it is unclear whether males can assess female fecundity before breeding. We carried out an experiment in which we measured variation in female fecundity (repeatability 39%, 213 females) in a captive zebra finch population, and tested whether males preferred unfamiliar females of high fecundity (approximately top 10% of the population; 30 eggs laid on average) over those of low fecundity (bottom 10%; 6 eggs). We first tested whether naïve human observers could identify the high-fecundity female when confronted with duos of high and low fecundity. Humans guessed correctly in 58% of the cases (95% CI 50%-66%) indicating that differences in female condition were not highly obvious to humans. Zebra finch males preferred the high-fecundity female in 59% of choice tests that lasted 20 min (CI 52%-66%). When extending such choice tests over several days, male “success” in associating with the high-fecundity female was still modest (61% correct choices, CI 44%-76%). Overall, male zebra finches seem to have only limited abilities to identify the better mate when faced with a choice between extremes in terms of female fecundity. We found no male preference for heavier females. We speculate that such a preference may not have evolved because, in contrast to many ectothermic species, predicting fecundity from female weight is not sufficiently accurate (r2 = 0.04) for the benefits to outweigh the costs of increased male-male competition for heavy females. Chapter 2:No mutual mate choice for quality in zebra finches: time to question a widely-held assumption Abstract: Studies of mate choice typically assume that individuals will prefer high quality mates and select them based on condition-dependent indicator traits. In species where both sexes invest substantially in parental care, mutual mate choice is expected to result in assortative mating for quality. When assortment is not perfect, the lower quality pair members are expected to compensate by increased parental investment in order to secure their partner (positive differential allocation). This framework has been assumed to hold for monogamous model species like the zebra finch (Taeniopygia guttata), but little positive evidence has emerged, maybe because of the difficulty of defining individual quality. By combining multiple measures of causes (inbreeding, early nutrition) and consequences (ornaments, displays, fitness components) of variation in quality into a single principal component, we here show that quality variation can be quantified successfully and it indeed predicts individual pairing success, presumably because it reflects an individual’s vigor or ability to invest in reproduction. Yet, despite high statistical power, we found no evidence for either assortative mating or for positive differential allocation. We suggest that zebra finch ornaments and displays are not sufficiently reliable for choosy individuals to obtain benefits from being selective about such traits that are greater than the costs of competition for the putative best partner. We call for unbiased quantification of preference strength and signal honesty and avoidance of selective reporting of significant results. Chapter 3: Irreproducible text-book ‘knowledge’: the effects of color bands on zebra finch fitness Abstract: Many fields of science – including behavioral ecology – currently experience a heated debate about the extent to which publication bias against null-findings results in a misrepresentative scientific literature. Here, we show a case of an extreme mismatch between strong positive support for an effect in the literature and a failure to detect this effect across multiple attempts at replication. For decades, researchers working with birds have individually marked their study species with colored leg bands. For the zebra finch Taeniopygia guttata, a model organism in behavioral ecology, many studies over the past 35 years have reported effects of bands of certain colors on male or female attractiveness and further on behavior, physiology, life-history and fitness. Only 8 out of 39 publications presented exclusively null-findings. Here, we analyze the results of eight experiments in which we quantified the fitness of a total of 730 color-banded individuals from four captive populations (two domesticated and two recently wild-derived). This sample size exceeds the combined sample size of all 23 publications that clearly support the “color-band effect” hypothesis. We found that band color explains no variance in either male or female fitness. We also found no heterogeneity in color-band effects, arguing against both context- and population-specificity. Analysis of unpublished data from three other laboratories strengthens the generality of our null finding. Finally, a meta-analysis of previously published results is indicative of selective reporting and suggests that the effect size approaches zero when sample size is large. We argue that our field – and science in general – would benefit from more effective means to counter confirmation bias and publication bias. Chapter 4: Scrutinizing assortative mating in birds Abstract: Pair bonds often form between individuals that resemble one another. Such assortative mating appears to be widespread not only in humans but also throughout the animal kingdom. Yet it remains usually unclear whether assortative mating arises primarily from mate choice (‘like attracts like’), from spatial or temporal separation, or from observer, reporting, publication and search bias. Here, we reveal how compelling meta-analytical evidence for size-assortative mating in birds (r = 0.201 ± 0.022 SE, 58 species, 15,971 pairs) vanishes gradually with increased control of confounding factors. Specifically, the effect size decreased to half when we estimated assortative mating from unpublished data (free of reporting and publication bias) of nine long-term field studies (r = 0.106 ± 0.048 SE, eight species, 16,611 pairs) and assortative mating nearly disappeared (to around r = 0.018) when both partners were measured by independent observers or separate in space and time. Finally, we found no evidence for assortative mating in a direct experimental test for mutual mate choice in captive populations of zebra finches (r = -0.003 ± 0.141 SE, 1,414 pairs). These results highlight the importance of unpublished data in generating unbiased meta-analytical conclusions, and suggest that the apparent ubiquity of assortative mating reported in the literature is overestimated and may typically not be driven by mate choice. Chapter 5: Genetic constraints of female promiscuity: male corollary or independent trajectory? Abstract: The question of why females of many socially monogamous species engage in copulations outside the social pair bond has intrigued behavioral ecologists for many decades, especially because the benefits of such promiscuous behavior often do not seem to outweigh the costs. Hence, models of genetic constraint have been proposed, where female promiscuity emerges as a genetic corollary of alleles that are either beneficial for male extra-pair mating success (intersexual pleiotropy hypothesis) or beneficial for female fecundity (intrasexual pleiotropy hypothesis). In a first empirical test using captive zebra finches we had found support for the former hypothesis, suggesting that artificial selection on male sex drive could alter female extra-pair mating behavior as a genetic corollary. Here, we directly follow up on this suggestion and re-examine both hypotheses after establishing selection lines for male sex drive. After testing for intersexual pleiotropy with much increased statistical power, we now have to revise our previous conclusions, because the new data does not confirm the idea that male and female promiscuity are genetically homologous traits. However, we find some support for the idea that female promiscuity is genetically correlated with female fecundity, calling for more empirical tests of the intrasexual pleiotropy hypothesis. We also find that female extra-pair mating behavior is strongly context dependent, rendering genetic studies difficult and suggesting that social network analyses might shed more light on when and why females mate outside the pair bond.
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Wang, Daiping
2019
English
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Wang, Daiping (2019): Mate choice and the evolution of female promiscuity in a socially monogamous species. Dissertation, LMU München: Faculty of Biology
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Abstract

Chapter 1: Male zebra fiches have limited ability to identify high-fecundity females Abstract: In species with bi-parental care and lifetime monogamy, the fecundity of a male’s partner can be a major component of his fitness, but it is unclear whether males can assess female fecundity before breeding. We carried out an experiment in which we measured variation in female fecundity (repeatability 39%, 213 females) in a captive zebra finch population, and tested whether males preferred unfamiliar females of high fecundity (approximately top 10% of the population; 30 eggs laid on average) over those of low fecundity (bottom 10%; 6 eggs). We first tested whether naïve human observers could identify the high-fecundity female when confronted with duos of high and low fecundity. Humans guessed correctly in 58% of the cases (95% CI 50%-66%) indicating that differences in female condition were not highly obvious to humans. Zebra finch males preferred the high-fecundity female in 59% of choice tests that lasted 20 min (CI 52%-66%). When extending such choice tests over several days, male “success” in associating with the high-fecundity female was still modest (61% correct choices, CI 44%-76%). Overall, male zebra finches seem to have only limited abilities to identify the better mate when faced with a choice between extremes in terms of female fecundity. We found no male preference for heavier females. We speculate that such a preference may not have evolved because, in contrast to many ectothermic species, predicting fecundity from female weight is not sufficiently accurate (r2 = 0.04) for the benefits to outweigh the costs of increased male-male competition for heavy females. Chapter 2:No mutual mate choice for quality in zebra finches: time to question a widely-held assumption Abstract: Studies of mate choice typically assume that individuals will prefer high quality mates and select them based on condition-dependent indicator traits. In species where both sexes invest substantially in parental care, mutual mate choice is expected to result in assortative mating for quality. When assortment is not perfect, the lower quality pair members are expected to compensate by increased parental investment in order to secure their partner (positive differential allocation). This framework has been assumed to hold for monogamous model species like the zebra finch (Taeniopygia guttata), but little positive evidence has emerged, maybe because of the difficulty of defining individual quality. By combining multiple measures of causes (inbreeding, early nutrition) and consequences (ornaments, displays, fitness components) of variation in quality into a single principal component, we here show that quality variation can be quantified successfully and it indeed predicts individual pairing success, presumably because it reflects an individual’s vigor or ability to invest in reproduction. Yet, despite high statistical power, we found no evidence for either assortative mating or for positive differential allocation. We suggest that zebra finch ornaments and displays are not sufficiently reliable for choosy individuals to obtain benefits from being selective about such traits that are greater than the costs of competition for the putative best partner. We call for unbiased quantification of preference strength and signal honesty and avoidance of selective reporting of significant results. Chapter 3: Irreproducible text-book ‘knowledge’: the effects of color bands on zebra finch fitness Abstract: Many fields of science – including behavioral ecology – currently experience a heated debate about the extent to which publication bias against null-findings results in a misrepresentative scientific literature. Here, we show a case of an extreme mismatch between strong positive support for an effect in the literature and a failure to detect this effect across multiple attempts at replication. For decades, researchers working with birds have individually marked their study species with colored leg bands. For the zebra finch Taeniopygia guttata, a model organism in behavioral ecology, many studies over the past 35 years have reported effects of bands of certain colors on male or female attractiveness and further on behavior, physiology, life-history and fitness. Only 8 out of 39 publications presented exclusively null-findings. Here, we analyze the results of eight experiments in which we quantified the fitness of a total of 730 color-banded individuals from four captive populations (two domesticated and two recently wild-derived). This sample size exceeds the combined sample size of all 23 publications that clearly support the “color-band effect” hypothesis. We found that band color explains no variance in either male or female fitness. We also found no heterogeneity in color-band effects, arguing against both context- and population-specificity. Analysis of unpublished data from three other laboratories strengthens the generality of our null finding. Finally, a meta-analysis of previously published results is indicative of selective reporting and suggests that the effect size approaches zero when sample size is large. We argue that our field – and science in general – would benefit from more effective means to counter confirmation bias and publication bias. Chapter 4: Scrutinizing assortative mating in birds Abstract: Pair bonds often form between individuals that resemble one another. Such assortative mating appears to be widespread not only in humans but also throughout the animal kingdom. Yet it remains usually unclear whether assortative mating arises primarily from mate choice (‘like attracts like’), from spatial or temporal separation, or from observer, reporting, publication and search bias. Here, we reveal how compelling meta-analytical evidence for size-assortative mating in birds (r = 0.201 ± 0.022 SE, 58 species, 15,971 pairs) vanishes gradually with increased control of confounding factors. Specifically, the effect size decreased to half when we estimated assortative mating from unpublished data (free of reporting and publication bias) of nine long-term field studies (r = 0.106 ± 0.048 SE, eight species, 16,611 pairs) and assortative mating nearly disappeared (to around r = 0.018) when both partners were measured by independent observers or separate in space and time. Finally, we found no evidence for assortative mating in a direct experimental test for mutual mate choice in captive populations of zebra finches (r = -0.003 ± 0.141 SE, 1,414 pairs). These results highlight the importance of unpublished data in generating unbiased meta-analytical conclusions, and suggest that the apparent ubiquity of assortative mating reported in the literature is overestimated and may typically not be driven by mate choice. Chapter 5: Genetic constraints of female promiscuity: male corollary or independent trajectory? Abstract: The question of why females of many socially monogamous species engage in copulations outside the social pair bond has intrigued behavioral ecologists for many decades, especially because the benefits of such promiscuous behavior often do not seem to outweigh the costs. Hence, models of genetic constraint have been proposed, where female promiscuity emerges as a genetic corollary of alleles that are either beneficial for male extra-pair mating success (intersexual pleiotropy hypothesis) or beneficial for female fecundity (intrasexual pleiotropy hypothesis). In a first empirical test using captive zebra finches we had found support for the former hypothesis, suggesting that artificial selection on male sex drive could alter female extra-pair mating behavior as a genetic corollary. Here, we directly follow up on this suggestion and re-examine both hypotheses after establishing selection lines for male sex drive. After testing for intersexual pleiotropy with much increased statistical power, we now have to revise our previous conclusions, because the new data does not confirm the idea that male and female promiscuity are genetically homologous traits. However, we find some support for the idea that female promiscuity is genetically correlated with female fecundity, calling for more empirical tests of the intrasexual pleiotropy hypothesis. We also find that female extra-pair mating behavior is strongly context dependent, rendering genetic studies difficult and suggesting that social network analyses might shed more light on when and why females mate outside the pair bond.