Building Babies - Chapter 16

In contrast to birds, male mammals rarely help to raise the offspring. Of all mammals, only among rodents, carnivores, and primates, males are sometimes intensively engaged in providing infant care (Kleiman and Malcolm 1981). Male caretaking of infants has long been recognized in nonhuman primates (Itani 1959). Given that infant care behavior can have a positive effect on the infant’s development, growth, well-being, or survival, why are male mammals not more frequently involved in “building babies”? We begin the chapter defining a few relevant terms and introducing the theory and hypotheses that have historically addressed the evolution of paternal care. We then review empirical findings on male care among primate taxa, before focusing, in the final section, on our own work on paternal care in South American owl monkeys (Aotus spp.). We conclude the chapter with some suggestions for future studies.Deutsche Forschungsgemeinschaft (HU 1746/2-1) Wenner-Gren Foundation, the L.S.B. Leakey Foundation, the National Geographic Society, the National Science Foundation (BCS-0621020), the University of Pennsylvania Research Foundation, the Zoological Society of San Dieg

Non-Independent Mate Choice in Humans: Deciphering and Utilizing Information in a Social Environment

Thesis (Ph.D.) - Indiana University, Psychology, 2010In mate choice, one must gather information to be able to ascertain the value of potential mates. This information can come from directly and independently gathered sources, by talking to each potential mate oneself, or through non-independent sources by monitoring the selections of others in one's local environment. In order for humans to be able to perform the latter, they need an adaptive mate choice mechanism that is able to accurately judge the romantic interest between others in their social environment. This ability to decipher romantic interest is uncovered in a series of studies using ecologically and externally valid stimuli of real mate choice interactions coming from speed-dating sessions. These studies demonstrate not only the presence of this ability in humans, but also the specific informative cues used when making these judgments. Furthermore, additional behavioral experimentation illustrates how humans could utilize this ability to inform their own mate choice decisions. By recognizing romantic interest between others, individuals are able to copy the selections of others, in a process known as mate-choice copying. This phenomenon is first described using a novel methodology, and then its nuances are uncovered regarding how age, attractiveness, other individual differences, and the strength of available information all affect who, when, and how an individual decides to copy the mate choice selections of others. This body of work describes how humans, in ways similar to many other animals living in social groups, utilize information coming from their social environment to adaptively guide their individual mate choice decisions

The significant role of post-pairing male behavior on the evolution of male preferences and female traits

Existing sexual selection theory postulates that a sufficiently large variation in female fecundity or other direct benefits are fundamental for generating male mate choice. In this study, we suggest that, in addition to pre-pairing preferences, choosy males can also have different post-pairing behaviors, a factor which has been comparatively overlooked by previous studies. We found that both male preferences and female traits could evolve much more easily than previously expected when the choosy males that paired with unpreferred females would allocate more efforts to seeking additional post-pairing mating opportunities. Furthermore, a costly female trait could evolve when there was a trade-off between seeking additional mating and paternal care investment within social pair for choosy males. Finally, a costly male preference and a costly female trait might still evolve and reach a stable polymorphic state in the population, which might give rise to a high variability in male choice and female traits in nature. We suggest that male mate choice may be even more common than expected, which needs to be verified empiricall

Male fidelity expressed through rapid testosterone suppression of ultrasonic vocalizations to novel females in the monogamous California mouse

The steroid hormone testosterone (T) is a well-known mediator of male sexual behavior in vertebrates. However, less is known about T's rapid effects on sexual behavior, particularly those involving ultrasonic vocalizations (USVs), a mode of communication that can influence mate acquisition in rodents. Using the monogamous California mouse, Peromyscus californicus, we tested whether T rapidly alters male USV production by giving T or saline injections to non-paired (sexually naïve) males and paired (paternally experienced and pair-bonded) males immediately prior to a brief exposure to an unrelated, novel female. Among non-paired males, no differences in the total number of USVs were observed; however, T increased the proportion of simple sweeps produced. Among paired males, T decreased the number of USVs produced, and this change was driven by a reduction in simple sweeps. These results suggest a differential rapid effect of T pulses between non-paired and paired males upon exposure to a novel female. Additionally, we observed a positive correlation in the production of USVs made between males and novel females, and this relationship was altered by T. Given the importance of USVs in sexual communication, our study supports an essential concept of monogamy in that mate fidelity is reinforced by decreased responsiveness to prospective mates outside of the pair bond. The central mechanism in pair bonded males that decreases their responsiveness to novel females appears to be one that T can trigger. This is among the first studies to demonstrate that T can inhibit sexually related behaviors and do so rapidly

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

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

Factors affecting the demography of a lek-mating bird: the greater prairie-chicken

Doctor of PhilosophyDepartment of BiologyBrett K. SandercockSexual selection via female choice and male-male aggression leads to elaboration of male traits. If male traits correlated with reproductive success are honest signals of male quality, survival costs may be associated with the expression of those traits. Testosterone (hereafter ‘T’) may enhance male breeding success, but T can also reduce immunocompetence and survival. Socially monogamous male birds with higher circulating T experience reproductive advantages, but the role of T in lek mating systems is largely unknown. To address these issues, I individually marked and conducted focal behavioral observations of greater prairie-chickens (Tympanuchus cupido) at five lek sites over a 5-year period. Females were fitted with radio-telemetry to monitor nesting success and survival. I examined the relationship between male traits and mating success using multinomial discrete choice models, a statistical method not previously applied to studies of sexual selection. Male mating success was highly skewed at greater prairie-chicken leks with 18.5% of males obtaining 87.2% of all successful copulations (n = 108 males; 85 copulations). Mating success was influenced most by male behavior, followed by several morphological attributes. The role of T was quantified using blood samples and by experimentally implanting a subset of males with T. T did not consistently affect mating success. Non-territorial males had lower T levels than territorial males. Among territory holders, T was unexpectedly negatively correlated with mating success. However, the odds of receiving a copulation were 4.3 times (0.42 to 45.3) greater for T-implanted males than males with sham implants. Future work should explore the interactions among the immune system, parasite load, and mating success of prairie-chickens. Annual survival of male prairie-chickens was not related to mating success, behavior, age or T level, suggesting there is no cost of increased male mating success. Like males, reproductive success of females was also highly skewed because < 10% of nests successfully hatched young. Comparisons of seasonal and annual survival rates indicate that females experience increased mortality during the breeding season relative to the nonbreeding season. Synthesis of field estimates of demographic parameters indicates prairie-chicken populations will decline without changes in rangeland management to reduce predator numbers or provide more nesting cover

Mating and Parental Care in Lake Tanganyika's Cichlids

Cichlid fishes of Lake Tanganyika display a variety of mating and parental care behaviors, including polygamous and monogamous mouthbrooding and substrate breeding, cooperative breeding, as well as various alternative reproductive tactics such as sneaking and piracy. Moreover, reproductive behaviors sometimes vary within species both in space and in time. Here, I survey reports on mating and parenting behaviors of Lake Tanganyika cichlid species and address the evolution of mating and parental care patterns and sexual dimorphism. Notes on measures of sexual selection intensity and the difficulties of defining mating systems and estimating selection intensities at species level conclude the essay