Emily H. DuVal

The opportunity for sexual selection: not mismeasured, just misunderstood

Evolutionary biologists have developed several indices, such as selection gradients (β) and the opportunity for sexual selection (Is), to quantify the actual and/or potential strength of sexual selection acting in natural or experimental populations. In a recent paper, Klug et al. (J. Evol. Biol.23, 2010, 447) contend that selection gradients are the only legitimate metric for quantifying sexual selection. They argue that Is and similar mating‐system‐based metrics provide unpredictable results, which may be uncorrelated with selection acting on a trait, and should therefore be abandoned. We find this view short‐sighted and argue that the choice of metric should be governed by the research question at hand. We describe insights that measures such as the opportunity for selection can provide and also argue that Klug et al. have overstated the problems with this approach while glossing over similar issues with the interpretation of selection gradients. While no metric perfectly characterizes sexual selection in all circumstances, thoughtful application of existing measures has been and continues to be informative in evolutionary studies.

COOPERATIVE DISPLAY AND LEKKING BEHAVIOR OF THE LANCE-TAILED MANAKIN (CHIROXIPHIA LANCEOLATA)

Abstract Male Lance-tailed Manakins (Chiroxiphia lanceolata) perform multi-male courtship displays for females. To characterize the behavioral repertoire and the lek spatial organization of this species, I observed lekking males on Isla Boca Brava, Chiriquí Province, Panamá. Breeding began in March and continued through June, though courtship displays were recorded as late as November. Males were active throughout the day at display areas on the dispersed lek. Display areas were spaced 102 ± 30 m apart and averaged 2,480 ± 1,060 m2 in area (range: 525–4,500 m2; n = 24 display areas). The behavioral repertoire of Lance-tailed Manakins included 11 dance display elements, 7 common vocalizations, and 2 types of male-male duet songs. Duet songs and multimale dances for females were cooperative efforts by male pairs and included display elements that were never performed during courtship displays by solitary males. However, males performed both cooperative and entirely solo displays for females that ended in successful copulation, which suggests that cooperation is not obligate in this species, at least on the level of individual displays. Two sonations, or nonvocal communicative sounds, were noted during courtship displays: low-amplitude pulses of noise produced in rapid sets of 7–30 clicks during slow flight displays, and a low-frequency woosh produced at the nadir of swoop displays. The Lance-tailed Manakin display repertoire provides information useful in comparative analyses of the origin and evolution of display behavior within the manakin clade and in studies of the adaptive consequences of individual behavior within this species. Exhibición Cooperativa y Comportamiento de Asambleas de Cortejo en Chiroxiphia lanceolata

Adaptive Advantages of Cooperative Courtship for Subordinate Male Lance-Tailed Manakins

Male lance‐tailed manakins (Chiroxiphia lanceolata) cooperate in complex courtship displays, but the dominant (alpha) partner monopolizes mating opportunities. This raises the question of why subordinates (betas) cooperate. Three nonexclusive hypotheses explain the adaptive basis of helping behavior by subordinate males: cooperation may increase (1) subordinates’ immediate reproductive success, (2) the reproductive success of close relatives, or (3) subordinates’ chances of future reproduction. I demonstrated that beta males rarely sired chicks and were unrelated to their alpha partners but received delayed direct benefits from cooperation; betas had an increased probability of becoming an alpha when compared to males that had not been betas. To investigate the mechanism by which betas attain these adaptive benefits, I examined betas’ success in replacing their alpha partners both in natural turnover events and when alphas were experimentally removed. Beta males did not consistently inherit alpha roles in the same territories where they served their beta tenure, arguing that queuing for status does not fully explain the benefits of cooperation for betas. Instead, betas may be apprenticing to develop effective and appropriate displays that enhance their subsequent success as alphas. Complex social affiliations appear to mediate selective pressure for cooperation in this species.

Cooperating to compete: altruism, sexual selection and causes of male reproductive cooperation

Competition among males for access to reproductive opportunities is a central tenet of behavioural biology that has critical implications for studies of mating systems, sexual selection and the evolution of numerous phenotypic traits. Given the expectation that males should compete vigorously for access to females, it may at first seem paradoxical that males in some species cooperate to reproduce, often resulting in the apparent sacrifice of direct fitness by some members of these cooperative partnerships. Because this form of cooperation lies at the interface between natural, sexual and kin selection, studies of the adaptive consequences of male reproductive cooperation may yield important insights into how complex and sometimes conflicting selective pressures shape individual behaviour. Here, we define and review examples of reproductive cooperation among male animals. We take an integrative approach to reviewing the potential causes of maleemale cooperation, including potential adaptive hypotheses, ecological correlates, phylogenetic patterns and physiological mechanisms. The impact of male reproductive cooperation on sexual selection theory is also discussed. We conclude by outlining several important directions for future research, including efforts to improve understanding of the ecological and demographic contexts in which male reproductive cooperation occurs. Collectively, such analyses promise to improve our understanding of multiple fundamental concepts in evolutionary biology. 2013 The Authors. Published on behalf of The Association for the Study of Animal Behaviour by Elsevier Ltd. All rights reserved.

Sexual selection in a lekking bird: the relative opportunity for selection by female choice and male competition

Leks are classic models for studies of sexual selection due to extreme variance in male reproductive success, but the relative influence of intrasexual competition and female mate choice in creating this skew is debatable. In the lekking lance-tailed manakin (Chiroxiphia lanceolata), these selective episodes are temporally separated into intrasexual competition for alpha status and female mate choice among alpha males that rarely interact. Variance in reproductive success between status classes of adult males (alpha versus non-alpha) can therefore be attributed to male–male competition whereas that within status largely reflects female mate choice. This provides an excellent opportunity for quantifying the relative contribution of each of these mechanisms of sexual selection to the overall opportunity for sexual selection on males (Imales). To calculate variance in actual reproductive success, we assigned genetic paternity to 92.3% of 447 chicks sampled in seven years. Reproduction by non-alphas was rare and apparently reflected status misclassifications or opportunistic copulations en route to attaining alpha status rather than alternative mating strategies. On average 31% (range 7–44%, n=6 years) of the total Imales was due to variance in reproductive success between alphas and non-alphas. Similarly, in a cohort of same-aged males followed for six years, 44–58% of the total Imales was attributed to variance between males of different status. Thus, both intrasexual competition for status and female mate choice among lekking alpha males contribute substantially to the potential for sexual selection in this species.

Social organization and variation in cooperative alliances among male lance-tailed manakins

In species where males form cooperative alliances for the purposes of reproduction, there may be considerable variation in the strength and size of alliances observed within one population. Male lance-tailed manakins, Chiroxiphia lanceolata, form long-term cooperative alliances to court females on group-occupied display areas. I investigated male status and alliance structure in a colour-banded population. Each display area was a group territory attended by multiple adult and subadult males. Alpha males were present at display areas more often than other males, performed solo courtship displays for females, and vocalized distinctively in paired displays. Alpha–beta pairs had high duetting association index values and performed two types of paired courtship displays for females. I combined these characteristics in a predictive logistic regression model to assess male status probabilistically when not all key behaviours were observed. Typically, one alpha and one beta male occupied each display area, but males also formed multiple alliances (one alpha paired with multiple high-ranking subordinates) or were solitary, with no distinct alliances. Both alliances and solitary alphas attracted females for courtship displays. Alphas were generally older than their beta partners, but age did not absolutely predict status. Individual alpha males were involved in different alliance types in different years, showing that alliance variation is not the result of fixed differences in individual strategies. Instead, variation apparently results from changing opportunities for partnership formation and territory acquisition.

AGE-BASED PLUMAGE CHANGES IN THE LANCE-TAILED MANAKIN: A TWO-YEAR DELAY IN PLUMAGE MATURATION

Abstract I investigated the relationship of plumage to age and sex in the Lance-tailed Manakin (Pipridae, Chiroxiphia lanceolata) in the lowlands of western Panama from 1999–2004. I captured birds in mist nets, categorized their plumages, examined them for molt, and followed them for several years to document plumage changes. Male Lance-tailed Manakins exhibited three distinct postjuvenal plumages. Males achieved definitive adult plumage through sequential changes that occurred in the same order as in other Chiroxiphia manakins. Definitive male plumage developed over the same time span as reported for C. caudata but one year faster than C. linearis. Juvenal male plumage was similar to that of females, and 5% of 226 females had plumage similar to formative male plumage. Genetic sexing verified that changes observed late in the formative male plumage unambiguously identified sex and age of individual birds. This information can be used in behavioral studies to identify the age of male Lance-tailed Manakins captured in any of the predefinitive plumage stages.

Variation in annual and lifetime reproductive success of lance-tailed manakins: alpha experience mitigates effects of senescence on siring success

The causes of variation in individual reproductive success over a lifetime are not well understood. In long-lived vertebrates, reproductive output usually increases during early adulthood, but it is difficult to disentangle the roles of development and learning on this gain of reproductive success. Lekking lance-tailed manakins provide an opportunity to separate these processes, as the vast majority of male reproduction occurs after a bird obtains alpha status and maintains a display area in the lek, but the age at which males achieve alpha status varies widely. Using 11 years of longitudinal data on age, social status and genetic siring success, I assessed the factors influencing variation in siring success by individuals over their lifetimes. The data show increases in annual reproductive success with both age and alpha experience. At advanced ages, these gains were offset by senescence in fecundity. Individual ontogeny, rather than compositional change of the population, generated a nonlinear relationship of breeding tenure with lifetime success; age of assuming alpha status was unrelated to tenure as a breeder, or success in the alpha role. Importantly, these findings suggest that social experience can mitigate the negative effects of senescence in older breeders.

Hormonal correlates of social status and courtship display in the cooperatively lekking lance-tailed manakin.

Though cooperative behavior has long been a focus of evolutionary biology, the proximate hormonal mechanisms underlying cooperative interactions remain poorly understood. Lance-tailed manakins (Chiroxiphia lanceolata) are tropical passerines that form long-term male-male partnerships and cooperate in paired male courtship displays. To elucidate patterns of natural hormonal variation in relation to cooperation and reproductive behavior, we examined circulating androgen levels of male lance-tailed manakins in relation to social status, display behavior, and time of year. We found significantly higher circulating androgen levels in alpha-ranked (breeding) males compared to non-alpha adult males in the population. Beta males, which participated in courtship displays but did not copulate, had androgen levels indistinguishable from those of unpaired adult males that never displayed for females, suggesting that an elevated concentration of plasma testosterone in tropical lekking birds may be associated primarily with copulatory behavior or other status-specific traits, and not the performance of courtship display. Androgens decreased throughout the breeding season for males of all status categories. Interestingly, alphas that displayed for females in the observation session prior to sampling had lower androgen levels than alphas that did not display for females. This pattern may result from female discrimination against alpha males at display areas with high levels of social conflict among males, as social disruption is linked to elevated testosterone in many species. However, recent change of a display partner was not related to alpha androgen levels. We discuss alternative explanations and the possible implications of these results, and generate several testable predictions for future investigations.

Female mating preferences and offspring survival: testing hypotheses on the genetic basis of mate choice in a wild lekking bird

Indirect benefits of mate choice result from increased offspring genetic quality and may be important drivers of female behaviour. ‘Good‐genes‐for‐viability’ models predict that females prefer mates of high additive genetic value, such that offspring survival should correlate with male attractiveness. Mate choice may also vary with genetic diversity (e.g. heterozygosity) or compatibility (e.g. relatedness), where the females genotype influences choice. The relative importance of these nonexclusive hypotheses remains unclear. Leks offer an excellent opportunity to test their predictions, because lekking males provide no material benefits and choice is relatively unconstrained by social limitations. Using 12 years of data on lekking lance‐tailed manakins, Chiroxiphia lanceolata, we tested whether offspring survival correlated with patterns of mate choice. Offspring recruitment weakly increased with father attractiveness (measured as reproductive success, RS), suggesting attractive males provide, if anything, only minor benefits via offspring viability. Both male RS and offspring survival until fledging increased with male heterozygosity. However, despite parent–offspring correlation in heterozygosity, offspring survival was unrelated to its own or maternal heterozygosity or to parental relatedness, suggesting survival was not enhanced by heterozygosity per se. Instead, offspring survival benefits may reflect inheritance of specific alleles or nongenetic effects. Although inbreeding depression in male RS should select for inbreeding avoidance, mates were not less related than expected under random mating. Although mate heterozygosity and relatedness were correlated, selection on mate choice for heterozygosity appeared stronger than that for relatedness and may be the primary mechanism maintaining genetic variation in this system despite directional sexual selection.