Sexual selection, alternative reproductive tactics and sexual conflict in collared lizards : integration of molecular and behavioral ecology.

Sexual selection theory often predicts that socially dominant males should sire more offspring than males adopting subordinate social tactics. However, it is often difficult to determine the extent to which this expected distribution of male reproductive success is influenced by intra- and intersexual selection. Using a combination of field behavioral studies and molecular genetic techniques, I first tested the extent to which observations of social and spatial behavior predicted the distribution of reproductive success among female collared lizards and males displaying alternative social tactics (territorial and non-territorial) during a single reproductive season. I also examined the strength of sexual selection acting on male morphological and behavioral traits. Contrary to expectations, male social status did not accurately predict patterns of reproductive success: non-territorial males obtained reproductive success equal to that of territorial males and females were highly promiscuous, mating with a similar number of territorial and non-territorial males, both within and among successive clutches. None of the traits that I examined were significant targets of sexual selection among non-territorial males. However, male snout-vent-length was under positive directional selection among territorial males. To test the generality of my earlier findings, I expanded my analyses to encompass three seasons to examine how the number of female mates and offspring sired among males varied with marked natural variation in the intensity of intra- and intersexual selection within and among seasons, and the influence of behavioral traits on male fitness. I also examined how the degree of female promiscuity varied with changes in the intensity of sexual selection and the influence of female promiscuity on offspring survivorship. Unexpectedly, results from all seasons confirmed that non-territorial males consistently mated with similar numbers of females and sired similar numbers of offspring as territorial males. Moreover, females were promiscuous in all three seasons with similar numbers of territorial and non-territorial males. However, promiscuity decreased offspring survivorship. Together, my results suggest that mating relationships among collared lizards contrast sharply with predictions from classical mating system theory and likely represent the outcome of sexual conflict. Both sexual conflict and the high reproductive success of non-territorial males appear to be promoted by the homogeneous and continuous topography of the semi-natural habitat at my study site, which differs markedly from the natural habitat of collared lizards

The effect of relatedness on mating behavior in the satin bowerbird (Ptilonorhynchus violaceus)

Behavior is a main component of sexual selection theory in which male competition and female mate choice influence the evolution of a species. Relatedness commonly affects behavioral interactions, but the potential for relatedness to influence sexual selection is often overlooked. Here I show that relatedness affects mating behaviors in satin bowerbirds. Bowerbirds are a model species for non-resource based mating systems in which males provide only sperm to females, and females are free to mate with their preferred males, typically resulting in high skews in male mating success. Males build stick structures (bowers) on the ground to attract, and copulate with, females. Males compete, in part, by destroying neighboring males' bowers. Females search among multiple adjacent bowers and then select subsets of these males for courtship and then copulation. Automated video monitoring of bowers allows identification of males that destroy bowers and females that visit bowers for courtship or copulation. Using microsatellite genetic markers to estimate relatedness, I show that paternity assignments based on observed copulations match the genetic sires of offspring, supporting the hypotheses that copulations occur only at bowers and that male reproductive success can be reliably estimated from observed copulations. Next, I report that competing males are less aggressive, in the form of bower destructions, towards relatives than non-relatives and that this restraining effect of relatedness on aggression favors the close spatial association of relatives' bowers. These results support the hypothesis that relatedness affects male competition and ability to maintain attractive displays for females. Lastly, I investigate the influence of relatedness on female mate choice. I show that females do not actively prefer or avoid relatives in mate choice. However, females bias the areas in which they search for mates to be inclusive of relatives and then mate randomly with respect to relatedness within their search areas, resulting in tendencies to mate with relatives in some years. This effect of relatedness on female mate searching may be due in part to the spatial association of related males, and highlights the influence of mate searching rather than active mate preferences on overall mate choice patterns

Sexual selection: Symmetry, inbreeding and mate choice in Trinidadian guppies

This thesis investigates whether asymmetry has a role in sexual selection in guppies. This is potentially interesting because it might illuminate whether the cues used in female mate choice correlate with male quality (the "good genes" hypothesis) or purely "aesthetic" choice. Guppies are well suited to investigations of mate choice as males have prominent sexual pigments which females use in mate choice decisions. Theory predicts that the symmetry of secondary sexual characters could indicate the quality of the male, as it is widely thought that fluctuating asymmetry (FA) is a sensitive indicator of developmental stress. Sexual coloration in guppies was found to be sensitive to genetic stress caused by-inbreeding. Several traits showed indications of inbreeding depression. Pigment areas and numbers of spots and colours all decreased with inbreeding. The response of different pigments was highly correlated with their importance to females in each population. Display rate and swimming performance also showed signs of inbreeding depression. The evidence on these traits is consistent with the "good genes" hypothesis. But there was no difference in pigment FA between inbred and control fish. This provides no evidence that genetic stress is reflected particularly well by FA. Females did not prefer outbred males, but preferred high display frequency above other cues. However, if display rate was controlled, females of both populations preferred males with symmetrical patterns when given choices between males differing in spot symmetry - but this is unusual FA as this concerned unpaired characters. Spot asymmetry showed no response to inbreeding and thus was a poor indicator of male condition. This cue appears to support the "aesthetic choice" hypothesis. Overall, this evidence suggests that most (but not all) traits preferred by females are good indicators of male quality. There was no evidence that any form of symmetry correlated with male condition

Signals of demographic expansion in Drosophila virilis

BACKGROUND: The pattern of genetic variation within and among populations of a species is strongly affected by its phylogeographic history. Analyses based on putatively neutral markers provide data from which past events, such as population expansions and colonizations, can be inferred. Drosophila virilis is a cosmopolitan species belonging to the virilis group, where divergence times between different phylads go back to the early Miocene. We analysed mitochondrial DNA sequence variation among 35 Drosophila virilis strains covering the species' range in order to detect demographic events that could be used to understand the present characteristics of the species, as well as its differences from other members of the group. RESULTS: Drosophila virilis showed very low nucleotide diversity with haplotypes distributed in a star-like network, consistent with a recent world-wide exponential expansion possibly associated either with domestication or post-glacial colonization. All analyses point towards a rapid population expansion. Coalescence models support this interpretation. The central haplotype in the network, which could be interpreted as ancestral, is widely distributed and gives no information about the geographical origin of the population expansion. The species showed no geographic structure in the distribution of mitochondrial haplotypes, in contrast to results of a recent microsatellite-based analysis. CONCLUSION: The lack of geographic structure and the star-like topology depicted by the D. virilis haplotypes indicate a pattern of global demographic expansion, probably related to human movements, although this interpretation cannot be distinguished from a selective sweep in the mitochondrial DNA until nuclear sequence data become available. The particular behavioural traits of this species, including weak species-discrimination and intraspecific mate choice exercised by the females, can be understood from this perspective

Casanovas are liars : behavioral syndromes, sperm competition risk, and the evolution of deceptive male mating behavior in live-bearing fishes [version 2; referees: 2 approved, 1 approved with reservations]

Male reproductive biology can by characterized through competition over mates as well as mate choice. Multiple mating and male mate choice copying, especially in internally fertilizing species, set the stage for increased sperm competition, i.e., sperm of two or more males can compete for fertilization of the female’s ova. In the internally fertilizing fish Poecilia mexicana, males respond to the presence of rivals with reduced expression of mating preferences (audience effect), thereby lowering the risk of by-standing rivals copying their mate choice. Also, males interact initially more with a non-preferred female when observed by a rival, which has been interpreted in previous studies as a strategy to mislead rivals, again reducing sperm competition risk (SCR). Nevertheless, species might differ consistently in their expression of aggressive and reproductive behaviors, possibly due to varying levels of SCR. In the current study, we present a unique data set comprising ten poeciliid species (in two cases including multiple populations) and ask whether species can be characterized through consistent differences in the expression of aggression, sexual activity and changes in mate choice under increased SCR. We found consistent species-specific differences in aggressive behavior, sexual activity as well as in the level of misleading behavior, while decreased preference expression under increased SCR was a general feature of all but one species examined. Furthermore, mean sexual activity correlated positively with the occurrence of potentially misleading behavior. An alternative explanation for audience effects would be that males attempt to avoid aggressive encounters, which would predict stronger audience effects in more aggressive species. We demonstrate a positive correlation between mean aggressiveness and sexual activity (suggesting a hormonal link as a mechanistic explanation), but did not detect a correlation between aggressiveness and audience effects. Suites of correlated behavioral tendencies are termed behavioral syndromes, and our present study provides correlational evidence for the evolutionary significance of SCR in shaping a behavioral syndrome at the species level across poeciliid taxa

Effects of habitat complexity on male socio-spatial behavior and mating system dynamics in collared lizards.

Territory defense typically involves costly behavioral tactics that may detract from mating opportunities and other fitness enhancing activities. Selection on males therefore is expected to result in their establishing territories and adopting behavior patterns that maximize mating opportunities while simultaneously minimizing costs of spatial defense, which may vary among microhabitat patches that differ in physical parameters such as size, shape, and structural complexity. Using field behavioral studies, I first tested the influence of microhabitat patch structure (simple versus complex) on social and spatial behavior in territorial and non-territorial male eastern collared lizards (Crotaphytus collaris). As a result of markedly different structural conditions in the two microhabitat types, I proposed two alternative sexual selection models to explain factors that may govern male behavior and fitness. Despite the relatively small size and narrow dimensions of simple microhabitats, lizards colonized both simple patches, resulting in high local densities. Nevertheless, some males still defended territories on simple patches, and they did so without initiating contests with rivals or giving broadcast displays more frequently than territorial individuals on complex patches. By contrast, territorial males on simple patches moved throughout their territories more, and also courted a greater number of females more frequently than territorial males on complex patches. Non-territorial males in the two microhabitat types did not differ in any of the social variables measured. Increased visibility owing to the relatively flat and unobstructed surface topography of simple patches appears to promote increased courtship opportunities, while at the same time allowing males to deter same-sex competitors without significantly increasing costly defensive behaviors. Moreover, prioritization of courtship in highly competitive neighborhoods suggests that male behavior is shaped more by opportunities to interact with females than by competition for intrasexual dominant social status, perhaps because proximity to females coupled with simple habitat structure promotes monopolization of female mates. Although sexual selection theory predicts that socially dominant males will sire more offspring than males adopting subordinate social tactics, increased structural complexity of microhabitats may compromise the ability of territory owners to detect non-territorial rivals and prevent them from mating with female residents. To test the hypothesis that the ability of males to monopolize matings with females is negatively related to the structural complexity of microhabitats, I used molecular genetic techniques to quantify reproductive success for territorial and non-territorial males in each microhabitat type. Consistent with this prediction, males defending territories on simple patches sired a greater proportion of the offspring produced by individual mates compared to territorial males on complex patches. Contrary to the expectation that increased mate monopolization by territorial males would decrease mating opportunities for non-territorial males, neither the total number of offspring sired, nor the number of female mates differed as a function of male social status on simple patches, most likely as a result of high local female densities. By contrast, territorial males on complex patches sired more offspring total than their non-territorial rivals, and also tended to mate with more females (but not statistically so). The observation that territorial males on simple microhabitats sired a larger proportion of the offspring produced by their female mates compared to territorial males on complex patches suggests that mate monopolization may be more feasible in microhabitats that are less structurally complex because they afford territory owners high visibility while also limiting undetected movement by non-territorial males. Higher levels of mate monopolization without increased defense costs suggests that territory defense may be more economical in structurally simple microhabitats. Because the simple human-constructed microhabitats at this study site mimic some features of the natural rock outcrops and washes on which the socio-spatial behavior of collared lizards evolved, these results are more similar to what might be expected in populations in natural habitats

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

COGNITIVE PERFORMANCE AND THE EVOLUTION OF MULTIPLE BEHAVIORAL DISPLAY TRAITS

Males of many species have complex behavioral sexual displays and it is possible that these displays indicate aspects about male quality because of their relationship with cognitive ability. However, the relationship between behavioral display traits, cognitive ability, and reproductive success has received little attention. Satin bowerbirds, Ptilonorhynchus violaceus, are an excellent species for studying this relationship because their complex male courtship suggests a selective advantage to individuals with superior cognitive abilities. Here I show that cognitive performance can have important effects on mating success and the quality of behavioral displays. First, I present males with two novel problem solving tests and find that males who are better at solving these problems have higher mating success, establishing a link between male cognitive ability and sexual attractiveness. Second, I add four additional cognitive tests to expand the diversity of cognitive abilities tested and construct two measures of general cognitive ability using these data: the scores from an analysis that best explains covariation among performance on the different cognitive tests (g), and the average rank score on these cognitive tests ("IQ"). I show that these measures of general cognitive ability, as well as the majority of the independent cognitive tests, are positively associated with mating success. Third, I construct a different composite measure of male cognitive ability using an analysis that determines the combination of cognitive traits that make males most successful in attracting females (f). I show that this measure is significantly associated with my measures of general cognitive ability, suggesting that evolution of cognitive ability in bowerbirds is possible if there is sufficient heritability. I construct three different aggregate measures of male display quality (produced from four behavioral display traits) and find that they are all associated with f and with mating success. Finally, I show some support for the hypothesis that separate display traits may indicate different aspects of male cognitive ability. These results suggest that behavioral display traits may have a special role in sexual selection because of their connection to cognitive ability. Overall, this research highlights the importance of considering the interrelationship between cognitive ability and sexual selection