Seth W. Coleman

Variable female preferences drive complex male displays.

Complexity in male sexual displays is widely appreciated but diversity in female mate choice has received little attention. Males of many species have sexual displays composed of multiple display traits, and females are thought to use these different traits in mate choice. Models of multiple display trait evolution suggest that these traits provide females with different kinds of information in different stages of the mate choice process, or function as redundant signals to improve the accuracy of mate assessment. We suggest that complex male displays might also arise because of variation in female preferences for particular male display traits. The causes of female preference variation have received little attention, and the role of preference variation in shaping complex male displays is unclear. Here we show that in satin bowerbirds (Ptilonorhynchus violaceus) female mate choice is a multistage process, where females of different ages use different male display traits in successive stages. Age- and stage-specific female preferences may contribute to explaining the widespread occurrence of multifaceted male displays.

Male satin bowerbirds, Ptilonorhynchus violaceus, adjust their display intensity in response to female startling: an experiment with robotic females

Females of many species preferentially mate with males that produce courtship displays at a high intensity or rate; however, males do not always display at their maximum intensity during courtship. Evidence suggests that this behaviour may be adaptive in satin bowerbirds, because overly intense displays can disrupt courtship by startling females. Females signal the display intensity that they will tolerate from a male; males that respond by adjusting their intensity reduce the likelihood of startling females and increase their courtship success. However, even the most responsive males occasionally startle females. When this occurs, males could avoid further threat to females by decreasing the intensity of their subsequent displays. We used robotic female bowerbirds that mimicked female startling to test the hypothesis that males reduce the intensity of their courtship displays after startling females. Supporting this hypothesis, males displayed at significantly lower intensity after robots were startled in experimental treatments than when they were not startled in control treatments. We found no evidence that the degree of male response to startling was related to male courtship success. In spite of evidence that female bowerbirds prefer the most intensely displaying males as mates, we found that males did not always display at maximum intensity, but rather reduced their intensity in response to female startling during courtship. Our results suggest that males adjust the level of expression of their display traits in response to female behaviours during courtship, and by doing so, males may increase their chances for successful courtship.

Female preferences drive the evolution of mimetic accuracy in male sexual displays.

Males in many bird species mimic the vocalizations of other species during sexual displays, but the evolutionary and functional significance of interspecific vocal mimicry is unclear. Here we use spectrographic cross-correlation to compare mimetic calls produced by male satin bowerbirds (Ptilonorhynchus violaceus) in courtship with calls from several model species. We show that the accuracy of vocal mimicry and the number of model species mimicked are both independently related to male mating success. Multivariate analyses revealed that these mimetic traits were better predictors of male mating success than other male display traits previously shown to be important for male mating success. We suggest that preference-driven mimetic accuracy may be a widespread occurrence, and that mimetic accuracy may provide females with important information about male quality. Our findings support an alternative hypothesis to help explain a common element of male sexual displays.

Co-option of male courtship signals from aggressive display in bowerbirds

The pre–existing trait hypothesis suggests that females evolve a mating preference for an already existing male trait. This hypothesis poses a simple resolution to Darwins long–standing question of how elaborate, male display traits evolve. The frequently observed convergence of aggressive and courtship displays across a wide array of species provides the only current support for this hypothesis. Here we provide much more detailed supporting evidence from bowerbird skrraa calls used in aggression and courtship. Consistent with the pre–existing trait hypothesis we show that (i) putatively co–opted skrraa calls used in courtship and aggression are homologous, (ii) skrraa calls were used in aggression in bowerbirds before being used in courtship, (iii) historically, intense, aggressive–like courtship calls were present near the time of co-option, and (iv) bower types contemporaneous with co–option emphasize design features that provide females protection from the adverse effects of intense courtship displays. These results, plus evidence for a female preference for males with intense aggressive–like courtship skrraa calls, suggest that aggressive skrraa calls have been co–opted for use in male courtship display.

Reduced opsin gene expression in a cave-dwelling fish

Regressive evolution of structures associated with vision in cave-dwelling organisms is the focus of intense research. Most work has focused on differences between extreme visual phenotypes: sighted, surface animals and their completely blind, cave-dwelling counterparts. We suggest that troglodytic systems, comprising multiple populations that vary along a gradient of visual function, may prove critical in understanding the mechanisms underlying initial regression in visual pathways. Gene expression assays of natural and laboratory-reared populations of the Atlantic molly (Poecilia mexicana) revealed reduced opsin expression in cave-dwelling populations compared with surface-dwelling conspecifics. Our results suggest that the reduction in opsin expression in cave-dwelling populations is not phenotypically plastic but reflects a hardwired system not rescued by exposure to light during retinal ontogeny. Changes in opsin gene expression may consequently represent a first evolutionary step in the regression of eyes in cave organisms.

Mourning dove ( Zenaida macroura ) wing-whistles may contain threat-related information for con- and hetero-specifics

Distinct acoustic whistles are associated with the wing-beats of many doves, and are especially noticeable when doves ascend from the ground when startled. I thus hypothesized that these sounds may be used by flock-mates as cues of potential danger. To test this hypothesis, I compared the responses of mourning doves (Zenaida macroura), northern cardinals (Cardinalis cardinalis), and house sparrows (Passer domesticus) to audio playbacks of dove ‘startle wing-whistles’, cardinal alarm calls, dove ‘nonstartle wing-whistles’, and sparrow ‘social chatter’. Following playbacks of startle wing-whistles and alarm calls, conspecifics and heterospecifics startled and increased vigilance more than after playbacks of other sounds. Also, the latency to return to feeding was greater following playbacks of startle wing-whistles and alarm calls than following playbacks of other sounds. These results suggest that both conspecifics and heterospecifics may attend to dove wing-whistles in decisions related to antipredator behaviors. Whether the sounds of dove wing-whistles are intentionally produced signals warrants further testing.

Swordtail fry attend to chemical and visual cues in detecting predators and conspecifics.

Predation pressure and energy requirements present particularly salient opposing selective pressures on young fish. Thus, fry are expected to possess sophisticated means of detecting predators and resources. Here we tested the hypotheses that fry of the swordtail fish Xiphophorus birchmanni use chemical and visual cues in detection of predators and conspecifics. To test these hypotheses we presented young (<7 day-old) fry with combinations of visual and chemical stimuli from adult conspecifics and predators. We found that exposure to predator odors resulted in shoal tightening similar to that observed when fry were presented with visual cues alone. In trials with conspecific stimuli, fry were particularly attracted to adult conspecifics when presented simultaneous visual and chemical stimuli compared to the visual stimulus alone. These results show that fry attend to the odors of adult conspecifics, whose presence in a particular area may signal the location of resources as well as an absence of predators. This is one of the first studies to show that such young fish use chemical and visual cues in predator detection and in interactions with conspecifics. Previous research in X. birchmanni has shown that anthropogenic alteration of the chemical environment disrupts intraspecific chemical communication among adults; we suggest that because fry use the same chemosensory pathways to detect predators and conspecifics, alteration of the chemical environment may critically disrupt predator and resource detection.

Aerobic capacity in wild satin bowerbirds: repeatability and effects of age, sex and condition

SUMMARY Individual variation in aerobic capacity has been extensively studied, especially with respect to condition, maturity or pathogen infection, and to gain insights into mechanistic foundations of performance. However, its relationship to mate competition is less well understood, particularly for animals in natural habitats. We examined aerobic capacity [maximum rate of O2 consumption () in forced exercise] in wild satin bowerbirds, an Australian passerine with a non-resource based mating system and strong intermale sexual competition. We tested for repeatability of mass and , differences among age and sex classes, and effects of several condition indices. In adult males, we examined interactions between aerobic performance and bower ownership (required for male mating success). There was significant repeatability of mass and within and between years, but between-year repeatability was lower than within-year repeatability. varied with an overall scaling to mass0.791, but most variance in was not explained by mass. Indicators of condition (tarsus and wing length asymmetry, the ratio of tarsus length to mass) were not correlated to . Ectoparasite counts were weakly correlated to across all age–sex classes but not within any class. Adult males, the cohort with the most intense levels of mating competition, had higher than juvenile birds or adult females. However, there was no difference between the of bower-owning males and that of males not known to hold bowers. Thus one major factor determining male reproductive success was not correlated to aerobic performance.

Reproductive Isolation, Reproductive Mode, and Sexual Selection: Empirical Tests of the Viviparity‐Driven Conflict Hypothesis

A central goal in evolutionary biology is to elucidate general mechanisms and patterns of species divergence. The viviparity‐driven conflict (VDC) hypothesis posits that intense mother‐embryo conflict associated with viviparity drives rapid reproductive isolation among viviparous species, is intensified by multiple paternity, and reduces female reliance on precopulatory cues in mate choice. We tested these predictions using comparisons of oviparous and viviparous fishes. Consistent with the VDC hypothesis, we found that, relative to oviparous species, only closely related viviparous fishes are known to hybridize. Also in support of the VDC hypothesis, we found that (1) elaborate male sexual ornamentation may be more common in viviparous species with relatively low levels of maternal provisioning of embryos compared with those with high levels of provisioning and (2) the degree of multiple paternity is higher in viviparous species than in oviparous species. In contrast to a prediction of the VDC hypothesis, we found no relationship between the degree of multiple paternity and elaborate male sexual ornamentation, although statistical power was quite low for this test. Whereas overall our results strongly support the central tenet of the VDC hypothesis—that reproductive mode affects rates of evolution of reproductive isolation and the strength of sexual selection—they cannot rule out two alternative models we propose that may also explain the observed patterns.

A field-study of inducible molecular defenses, ultraviolet radiation, and melanomagenesis in natural Xiphophorus hybrids

Ultraviolet radiation—the primary natural pollutant affecting melanomagenesis—may represent a widespread ecological stressor for many fishes, and yet the relationship between UV-exposure and stress has not been investigated in natural fish populations. Recent lab-based studies have sought to characterize the relationship between tumorigenesis and the induction of molecular defenses, such as heat shock proteins. Here we show that ultraviolet radiation and heat shock protein gene expression explain a significant amount of the variation in hyper-melanization—the phenotypic precursor to melanoma—in wild hybrids of Xiphophorus, laboratory models in cancer research. Our results suggest exposure to UV radiation causes stress which induces molecular defense mechanisms, which in turn may facilitate tumorigenesis in natural fish populations. Studies of laboratory-based model organisms in natural settings, like this one, may provide important insights into ecological and evolutionary relationships obscured in controlled laboratory environments. We hope that ours is only the first of many studies to investigate the such relationships between environmental stress, stress-induced molecular defenses, and cancer in fishes.