Mate Choice Trials Research Articles

The genetics of mate preferences in hybrids between two young and sympatric Lake Victoria cichlid species.

The genetic architecture of mate preferences is likely to affect significant evolutionary processes, including speciation and hybridization. Here, we investigate laboratory hybrids between a pair of sympatric Lake Victoria cichlid fish species that appear to have recently evolved from a hybrid population between similar predecessor species. The species demonstrate strong assortative mating in the laboratory, associated with divergent male breeding coloration (red dorsum versus blue). We show in a common garden experiment, using DNA-based paternity testing, that the strong female mate preferences among males of the two species are fully recovered in a large fraction of their F2 hybrid generation. Individual hybrid females often demonstrated consistent preferences in multiple mate choice trials (more than or equal to five) across a year or more. This result suggests that female mate preference is influenced by relatively few major genes or genomic regions. These preferences were not changed by experience of a successful spawning event with a male of the non-preferred species in a no-choice single-male trial. We found no evidence for imprinting in the F2 hybrids, although the F1 hybrid females may have been imprinted on their mothers. We discuss this nearly Mendelian inheritance of consistent innate mate preferences in the context of speciation theory.

Testosterone Reduces Promiscuity of Female Blue Tits (Cyanistes caeruleus): An Experimental Study

AbstractIn many animal species, extra‐pair copulations (EPCs) are common and can increase fitness in both sexes. In males, EPCs can increase total reproductive output, whereas in females benefits of EPCs can be indirect through improving the genetic quality of their offspring. Males and females of many vertebrates show an increase in levels of the hormone testosterone (T) during the mating period. In males, T plays an important role in regulating mating behaviour including increasing their EPC rate. While much is known about the role of T in male mating behaviour, the role of T in female reproduction remains unclear. To study the influence of T on extra‐pair paternity rates in females in a field setting, we created three experimental groups of female blue tits (Cyanistes caeruleus): treated with either T, flutamide (Flu; an androgen receptor blocker) or empty implants before egg laying. Subsequently, we scored the number of extra‐pair offspring (EPO) in their broods. We also assessed the attractiveness of females treated with either T or Flu to males in mate choice trials in the laboratory. The overall proportion of EPO was lower for the T‐implanted group compared with the control group, whereas Flu had no effect. Given that males did not show a preference for Flu‐ vs. T‐treated females in the mate choice trials, it appears less likely that the reduction in EPO in the T‐implanted females was due to a reduction in their attractiveness. T levels may have negatively influenced EPO rate by affecting female within‐pair and/or extra‐pair mating behaviour. Future behavioural studies should investigate how elevated T levels reduce the number of EPO.

Disruptive selection on male reproductive polymorphism in a jumping spider, Maevia inclemens

Genetic polymorphism in males has long been considered paradoxical because sexual selection is expected to deplete additive genetic variation. Although studies have shown how divergent selection between populations can make that work, it is very rare to find disruptive selection within one population. Since intersexual selection can have a significant effect on the phenotypic morphospace of the opposite sex, we analysed the role of female preference as a disruptive selective force. In this study we evaluated how female preference acts on anatomical and sex-related behavioural traits of two male morphs in the jumping spider Maevia inclemens. We used mate choice trials to analyse how female preference for the two morphs varied. The tests indicated that females preferred opposite values of two anatomical and two behavioural traits for each male morph. This study is, to our knowledge, the first to show disruptive sexual selection in Arachnidae and significantly expands the realm of disruptive selection, by adding one more case to the very few documented instances. These processes, which act entirely within a species, are of particular interest because they could contribute to the evolution of reproductive isolation and sympatric speciation by sexual selection, a controversial topic in evolutionary biology.

The behavioural effects of supplementing diets with synthetic and naturally sourced astaxanthin in an ornamental fish (Puntius titteya)

Carotenoids are routinely incorporated into ornamental fish diets with the aim of enhancing companion fish colouration which may concomitantly affect fish behaviour. Previously, colour enhancement has typically been achieved using synthetic carotenoids, however, there is now growing public demand for food additives such as carotenoids to be derived from natural sources, which can be acquired from microalgae and cyanobacteria. There has been very little research into whether natural carotenoids alter fish behaviour in a similar way to synthetic carotenoids; the present study aimed to determine whether behavioural changes typically associated with increased carotenoid consumption differed according to carotenoid source in the cherry barb (Puntius titteya). Cherry barbs were fed one of four diets (carotenoid-free, 20ppm synthetic astaxanthin (AX) sourced from Carophyll pink®, 20 or 40ppm of natural-AX sourced from Panaferd) over a 12 week period and then observed for colour changes, mate-choice and aggressive behaviours. The diets containing 20ppm synthetic-AX and natural-AX enhanced male red colouration of the anal fin and anterior dorsal area, via a reduction in hue, in comparison to the carotenoid-free control diet whereas only the 20ppm natural-AX altered the hue of female colour. In the mate choice trials, males spent more time with females fed the 20ppm synthetic-AX and 40ppm natural-AX compared with the carotenoid-free control and 20ppm natural AX. Experiments conducted under red-blocking and UV blocking conditions demonstrated an effect of red colouration and ultraviolet reflectance on mate discrimination. Interestingly, males fed both the synthetic and natural AX diets reduced aggressive interactions with a mirror image, even though they displayed enhanced red colouration, which is often used by fish as a signal of increased competitive ability. In conclusion, source of dietary AX affected the behaviour of cherry barbs, to the extent that synthetic AX exerted a stronger effect on mate-choice behaviour under full spectrum lighting in comparison to a similar concentration of natural AX. This therefore demonstrates that the behaviour of companion fish can be influenced by the source of carotenoids within their food.

Male personality and female spawning consistency in a goby with exclusive male care

Consistent inter-individual behavioral differences in animals, or animal personalities, are increasingly recognized as an important component of sexual selection. Despite growing evidence for personality-mediated effects on reproductive success in species with biparental care, the link between personality and intrasexual competition or mate choice in species with uniparental care remains largely unexplored. Here, the non-caring sex in particular should seek partners with personality traits that promise high quality care. Therefore, we investigated effects of male personality in the common goby, a well-established model species for sexual selection under exclusive male care. Using competitive trials, we investigated how personality affects male ability to monopolize either of two central reproductive resources, nesting sites (male-male competition) and ready-to-spawn females (female choice). Personalities were scored in a feeding context and thus independent of reproduction. We found that slow-feeding individuals better succeeded in monopolizing nests, but that female spawning decisions were independent of the foraging personality of two male competitors. Instead, females showed a remarkably consistent between-female spawning preference for slightly heavier males and males with more elaborate nests. Our findings indicate that fitness benefits of the male personality type only materialize via male-male competition in environments where nesting sites are a limiting resource, whereas female choice favors large males with elaborate nests independent of male personality. Animal personality can strongly affect reproductive success in species with parental care. We studied this link in the common goby, a fish where males build nests and solely take care of the brood until hatching. Hence, females should choose a male whose personality traits promise high quality care. We scored male personalities and conducted nest-competition and mate-choice trials. We found that male personality had an effect on nest monopolization, but not on female mating preferences. Instead, females agreed remarkably well in their mating decisions and consistently favored large males with elaborate nests. Our results show that male personality is important for nest allocation, which is crucial in environments where nesting sites are rare.

Mate Choice Drives Evolutionary Stability in a Hybrid Complex.

Previous studies have shown that assortative mating acts as a driver of speciation by countering hybridization between two populations of the same species (pre-zygotic isolation) or through mate choice among the hybrids (hybrid speciation). In both speciation types, assortative mating promotes speciation over a transient hybridization stage. We studied mate choice in a hybrid vertebrate complex, the allopolyploid fish Squalius alburnoides. This complex is composed by several genomotypes connected by an intricate reproductive dynamics. We developed a model that predicts the hybrid complex can persist when females exhibit particular mate choice patterns. Our model is able to reproduce the diversity of population dynamic outcomes found in nature, namely the dominance of the triploids and the dominance of the tetraploids, depending on female mate choice patterns and frequency of the parental species. Experimental mate choice trials showed that females exhibit the preferences predicted by the model. Thus, despite the known role of assortative mating in driving speciation, our findings suggest that certain mate choice patterns can instead hinder speciation and support the persistence of hybrids over time without speciation or extinction.

A Potential Case of Reinforcement in a Facultatively Sexual Unicellular Eukaryote.

The origin of a new species requires a mechanism to prevent divergent populations from interbreeding. In the classic allopatric model, divided populations evolve independently and accumulate genetic differences. If contact is restored, hybrids suffer reduced fitness and selection may favor traits that prevent mistakes in mating, a process known as reinforcement. This decisive but transient phase is challenging to document and has been reported mostly in macroorganisms. Very little is known about the processes through which new microbial species originate. In particular, it is unclear whether microbial eukaryotes, many of which can reproduce sexually during complex life cycles, speciate in much the same way as do well-studied plants and animals. Using individual cellular mate choice trials, we investigated the mating behavior of sympatric and allopatric woodland populations of the yeast Saccharomyces paradoxus. We find evidence consistent with reinforcement, potentially representing an example of microbial speciation in progress.

Conspicuous female ornamentation and tests of male mate preference in threespine sticklebacks (Gasterosteus aculeatus).

Sexual selection drives the evolution of exaggerated male ornaments in many animal species. Female ornamentation is now acknowledged also to be common but is generally less well understood. One example is the recently documented red female throat coloration in some threespine stickleback (Gasterosteus aculeatus) populations. Although female sticklebacks often exhibit a preference for red male throat coloration, the possibility of sexual selection on female coloration has been little studied. Using sequential and simultaneous mate choice trials, we examined male mate preferences for female throat color, as well as pelvic spine color and standard length, using wild-captured threespine sticklebacks from the Little Campbell River, British Columbia. In a multivariate analysis, we found no evidence for a population-level mate preference in males, suggesting the absence of directional sexual selection on these traits arising from male mate choice. Significant variation was detected among males in their preference functions, but this appeared to arise from differences in their mean responsiveness across mating trials and not from variation in the strength (i.e., slope) of their preference, suggesting the absence of individual-level preferences as well. When presented with conspecific intruder males, male response decreased as intruder red throat coloration increased, suggesting that males can discriminate color and other aspects of phenotype in our experiment and that males may use these traits in intrasexual interactions. The results presented here are the first to explicitly address male preference for female throat color in threespine sticklebacks.

Males Benefit from Mating with Outbred Females in Drosophila littoralis: Male Choice for Female Genetic Quality?

AbstractThe evolution and expression of mate choice behaviour in either sex depends on the sex‐specific combination of mating costs, benefits of choice and constraints on choice. If the benefits of choice are larger for one sex, we would expect that sex to be choosier, assuming that the mating costs and constraints on choice are equal between sexes. Because deliberate inbreeding is a powerful genetic method for experimental manipulation of the quality of study organisms, we tested the effects of both male and female inbreeding on egg and offspring production in Drosophila littoralis. Female inbreeding significantly reduced offspring production (mostly due to lower egg‐to‐adult viability), whereas male inbreeding did not affect offspring production (despite a slight effect of paternal inbreeding on egg‐to‐adult viability). As inbreeding depressed female quality more than male quality, the benefits of mate choice were larger for males than for females. In mate choice experiments, inbreeding did not affect male mating success (measured as a probability to be accepted as a mate in a large group), suggesting that females did not discriminate among inbred and outbred males. In contrast, female mating success was affected by inbreeding, with outbred females having higher mating success than inbred females. This result was not explained by lower activity of inbred females. Our results show that D. littoralis males benefit from mating with outbred females of high genetic quality and suggest adaptive male mate choice for female genetic quality in this species. Thus, patterns of mating success in mate choice trials mirrored the benefits of choice: the sex that benefited more from choice (i.e. males) was more choosy.

Variable environmental effects on a multicomponent sexually selected trait.

Multicomponent signals are made up of interacting elements that generate a functional signaling unit. The interactions between signal components and their effects on individual fitness are not well understood, and the effect of environment is even less so. It is usually assumed that color patterns appear the same in all light environments and that the effects of each color are additive. Using guppies, Poecilia reticulata, we investigated the effect of water color on the interactions between components of sexually selected male coloration. Through behavioral mate choice trials in four different water colors, we estimated the attractiveness of male color patterns, using multivariate fitness estimates and overall signal contrast. Our results show that females exhibit preferences that favor groups of colors rather than individual colors independently and that each environment favors different color combinations. We found that these effects are consistent with female guppies selecting entire color patterns on the basis of overall visual contrast. This suggests that both individuals and populations inhabiting different light environments will be subject to divergent, multivariate selection. Although the appearance of color patterns changes with light environment, achromatic components change little, suggesting that these could function in species recognition or other aspects of communication that must work across environments. Consequently, we predict different phylogenetic patterns between chromatic and achromatic signals within the same clades.

A trade-off between natural and sexual selection underlies diversification of a sexual signal

A longstanding in evolutionary biology is that trade-offs between natural and sexual often underlie the diversification of sexual signals in the wild. A classic example of this selection trade-off hypothesis proposes that males evolve elaborate and conspicuous ornamentation in low-risk environments where female preferences dominate on sexual traits, but they evolve muted and relatively cryptic sexual traits in high-risk environments where from predators acts against conspicuous sexual traits and female preferences potentially weaken or reverse. However, little direct empirical evidence supports this notion. Using the model system of Bahamas mosquitofish (Gambusia hubbsi)—where males have recently evolved greater orange coloration in their dorsal fins in blue holes lacking predatory fish relative to populations with fish predators—we tested this using fish replicas differing only in dorsal-fin color. Specifically, we employed plastic fish models in a combination of field and lab experiments to directly examine conspicuity to predators and female preferences for dorsal-fin color. We found that orange-shifted dorsal fins resembling the color exhibited in predator-free populations appeared more conspicuous to predatory bigmouth sleepers (Gobiomorus dormitor) that are evolutionarily naive to mosquitofish. Wild-caught female mosquitofish preferred the orange-shifted dorsal-fin model during dichotomous choice tests; evolutionary history with predators did not affect female preferences. Similar mate-choice trials with lab-born virgin females also found preferences for the orange-shifted dorsal-fin model and revealed significant genetic variation for female preferences. Our study provides direct empirical evidence documenting a trade-off between natural and sexual in a colorful sexual signal.

Mating success is predicted by the interplay between multiple male and female traits in the small hairy maggot blowfly

Intersexual selection drives the evolution of reproductive traits, including ornamentation and courtship behaviour. However, most studies attempting to explain the relationships between reproductive traits are oversimplified because traits are evaluated independently, and assessment of mate choice is restricted to one sex. Further research is required to understand the extent to which interactions between traits influence mating decisions in both sexes. The small hairy maggot blowfly, Chrysomya varipes, offers an ideal opportunity to examine how interactions between foreleg ornamentation (males have conspicuous white and black hairs, whereas females have only black hairs) and complex courtship behaviour influence mating success in males and females. This study involved mate choice trials between single females and males that varied in foreleg ornamentation. Courtship investment was quantified for males, and ornamentation and body size were quantified for both sexes. Mating success was predicted by time invested in courtship, but not by either male and female ornamentation or body size alone. However, there was a significant interaction between courtship investment, ornamentation and body size. At any given courtship investment, males with more ornamentation had an increased probability of mating success. Females with more ornamentation also had an increased probability of mating success, because males invested more courtship in more ornamented females. Furthermore, the lightest males had an increased probability of mating success compared to the heaviest males, as lighter males invested more in courtship. Female weight, however, did not significantly affect the probability of mating. The results suggest that male foreleg ornamentation in C. varipes acts as an amplifier of the visual courtship display, adding to a small but growing body of evidence that multiple male and female traits can interact to influence mating decisions.

Incomplete behavioural isolation and asymmetric female preference in darter sister species (Percidae: Etheostoma)

In this study, female preferences and behavioural isolation were estimated in a pair of allopatric sister species, Etheostoma duryi and Etheostoma flavum. Dichotomous mate preference trials were conducted to determine whether females prefer to associate with conspecific over heterospecific males and free-spawning assays were conducted to determine whether those preferences translated into behavioural isolation. Dichotomous mate choice trials revealed asymmetric female preference, as female E. flavum preferred conspecific males, whereas female E. duryi showed no preference. Free-spawning assays indicated that behavioural isolation remains incomplete between E. duryi and E. flavum (IB = 0·19). In addition to female mating preferences, male behaviour also appeared to influence mating outcomes as male E. flavum consistently courted conspecific females more often in free-spawning assays whereas male E. duryi did not. The data therefore suggest that despite marked divergence in male nuptial colour, divergence in female preferences between these species may not be sufficient to maintain species boundaries upon secondary contact. These results contrast with similar work in a sympatric darter species pair and may be explained by considering the contributions of reinforcement and differences in colour pattern as well as colour value.

Mate choice by males and paternity distribution in offspring of triple-mated females in Neptunea arthritica (Gastropoda: Buccinidae)

Males of Neptunea arthritica have been shown to mate preferentially with copulated females (CFs) over noncopulated females, which is unexpected due to the increased risk of sperm competition. To investigate how this preference for CFs affects the reproductive success of males, paternity was examined in the offspring of 13 females that had each copulated with three different males following male mate-choice trials. The paternity of each offspring was assigned to its most likely sire using polymorphic microsatellite markers. Males consistently chose CFs. During intromission in the females’ second and third matings, live sperm cells were detected in the mucus exiting the female shell whereas no sperm were detected during the first matings. In the 13 analysed clutches, single paternity was found in seven clutches, dual paternity was found in three and triple paternity was found in three. These results suggest that males can achieve considerable reproductive success with a mated female through sperm removal.

Hatching asynchrony can have long-term consequences for offspring fitness in zebra finches under captive conditions

Hatching asynchrony can have profound short-term consequences for offspring, although the long-term consequences are less well understood. The purpose of this study was to examine the long-term consequences of hatching asynchrony for offspring fitness in birds. Specifically, we aimed to test the hypothesis that hatching asynchrony increases the sexual attractiveness and fecundity, respectively, of early-hatched male and female zebra finch, Taeniopygia guttata (Vieillot, 1817) offspring. Mate-choice trials comparing male nestlings with the same parents, but that were reared in asynchronous or experimentally synchronous broods, revealed no female preference in relation to hatching regime. We did however find strong evidence that, as adults, late-hatched males were more attractive to females than siblings that had hatched earlier. Meanwhile, we found a weak trend towards early-hatched females depositing more carotenoids and retinol in the egg yolk than late-hatched or synchronously hatched females, although there were no differences in terms of clutch characteristics or the deposition of α-tocopherol or γ-tocopherol in the egg yolk. Therefore, we found that the beneficial long-term consequences of hatching asynchrony were sex specific, being accrued by late-hatched male nestlings and by early-hatched female nestlings. Consequently, we conclude that the long-term consequences of hatching asynchrony are more complex than previously realised.

Spawning coloration, female choice and sperm competition in the redside dace, Clinostomus elongatus

Understanding pre- and postcopulatory mechanisms of sexual selection (male–male competition and female choice) can provide insight into the evolution of male ornamentation. In this study, we use an integrative approach to study sexual selection by incorporating measures of both mechanisms using the redside dace, Clinostomus elongatus, a freshwater, externally fertilizing fish found in streams of eastern North America. We measured the success of individual male redside dace in both pre- and postspawning sexual selection and related the success of males to a range of traits, including spectral properties and the size of their red spawning coloration, body size metrics and sperm quality. We found significant sexual dimorphism in the relative amount and spectral properties (saturation and brightness) of the red spawning coloration, with males being more ornamented than females. Using dichotomous mate choice trials, we found that females did not favour males with relatively larger red spawning coloration area and more saturated or brighter red spawning coloration. Males with relatively more red spawning area would be favoured in male–male postspawning sperm competition because they possess sperm with higher velocity, and sperm velocity was determined to be the key predictor of sperm competition success as assessed by paternity analyses related to in vitro sperm competition trials. These results suggest that prespawning selection via female choice is not driving the evolution of red spawning coloration and that postspawning selection via male–male competition is primarily determined by sperm velocity, which was correlated with the relative amount of red spawning coloration.

Mate choice plasticity in the field cricket Teleogryllus oceanicus: effects of social experience in multiple modalities

Social experience can elicit phenotypically plastic changes in mate choice, but little is known about the degree to which social information from one modality can influence mating decisions based on information from a different modality. I used the field cricket Teleogryllus oceanicus to test whether experience of chemical cues mimicking a high density of sexually mature males causes changes in mate choice based on acoustic signals. T. oceanicus males produce long-range calling songs to attract females for mating, but they also produce waxy, non-volatile hydrocarbons on their cuticle (CHCs) which, when deposited on a substrate, can be detected by females and may provide demographic information. I manipulated female experience of substrate-bound male CHCs and then performed acoustic mate choice trials. When CHCs were present on the substrate during trials, females showed greater motivation to respond to male calling song. This effect diminished with repeated exposure to male songs, demonstrating that the importance of olfactory cues in altering acoustic mate choice decreased with increasing exposure to acoustic signals. However, the temporal nature of CHC experience mattered: previous experience of CHCs did not alter subsequent female choice for male calling song traits. Exposure to male song increased the threshold of mate acceptance over time, and individuals varied considerably in overall levels of responsiveness. Taken together, the results demonstrate that mate choice is dependent on social context mediated by multiple modalities in T. oceanicus, but they do not support the idea that prior experience of social cues in one modality necessarily influences later mating decisions based on other signalling modalities.

Automated Interactive Video Playback for Studies of Animal Communication

Video playback is a widely-used technique for the controlled manipulation and presentation of visual signals in animal communication. In particular, parameter-based computer animation offers the opportunity to independently manipulate any number of behavioral, morphological, or spectral characteristics in the context of realistic, moving images of animals on screen. A major limitation of conventional playback, however, is that the visual stimulus lacks the ability to interact with the live animal. Borrowing from video-game technology, we have created an automated, interactive system for video playback that controls animations in response to real-time signals from a video tracking system. We demonstrated this method by conducting mate-choice trials on female swordtail fish, Xiphophorus birchmanni. Females were given a simultaneous choice between a courting male conspecific and a courting male heterospecific (X. malinche) on opposite sides of an aquarium. The virtual male stimulus was programmed to track the horizontal position of the female, as courting males do in the wild. Mate-choice trials on wild-caught X. birchmanni females were used to validate the prototype's ability to effectively generate a realistic visual stimulus.

Automated Interactive Video Playback for Studies of Animal Communication

Video playback is a widely-used technique for the controlled manipulation and presentation of visual signals in animal communication. In particular, parameter-based computer animation offers the opportunity to independently manipulate any number of behavioral, morphological, or spectral characteristics in the context of realistic, moving images of animals on screen. A major limitation of conventional playback, however, is that the visual stimulus lacks the ability to interact with the live animal. Borrowing from video-game technology, we have created an automated, interactive system for video playback that controls animations in response to real-time signals from a video tracking system. We demonstrated this method by conducting mate-choice trials on female swordtail fish, Xiphophorus birchmanni. Females were given a simultaneous choice between a courting male conspecific and a courting male heterospecific (X. malinche) on opposite sides of an aquarium. The virtual male stimulus was programmed to track the horizontal position of the female, as courting males do in the wild. Mate-choice trials on wild-caught X. birchmanni females were used to validate the prototype's ability to effectively generate a realistic visual stimulus.

The cost of mating and mutual mate choice in 2 role–reversed honey locust beetles

Situations where both males and females simultaneously exercise mate choice may be much more common than previously believed. Yet, experimental studies of mutual mate choice are rare as is information on the types of female traits that are favored by male mate choice. We first assessed the cost of mating to males under different feeding regimes in 2 honey locust beetles (Bruchidae, Megabruchidius spp.) where females actively search for and court males. Further, in a series of mate choice trials, we manipulated female mating status and male food provisioning to assess how male and female characteristics affected the outcome of male–female interactions. Mating carried substantial costs to males, but these costs were independent of food availability. Males generally showed a preference for large females but also for females that delivered a more vigorous courtship display. Moreover, males preferred virgin females in one species but nonvirgin females in the other species, and we provide data suggesting that this choice is adaptive. Female choice was restricted to a lower rate of female mate rejection of larger males in one of the species. Our results reveal a striking interspecific variation in mutual mate choice, even between these closely related species, and show that sexual selection in females can act on much the same types of traits that are commonly considered sexually selected in males, such as size-related traits and courtship vigor. This suggests that a preference for condition-dependent traits may be a commonality that is shared between mate choice by both sexes. Key words: allometry, Bruchidae, mate choice, nuptial gifts, sex-role reversal, sexual selection. [Behav Ecol]