Variation In Female Preferences Research Articles

How to generate and test hypotheses about colour: insights from half a century of guppy research.

Coloration facilitates evolutionary investigations in nature because the interaction between genotype, phenotype and environment is relatively accessible. In a landmark set of studies, Endler addressed this complexity by demonstrating that the evolution of male Trinidadian guppy coloration is shaped by the local balance between selection for mate attractiveness versus crypsis. This became a textbook paradigm for how antagonistic selective pressures may determine evolutionary trajectories in nature. However, recent studies have challenged the generality of this paradigm. Here, we respond to these challenges by reviewing five important yet underappreciated factors that contribute to colour pattern evolution: (i) among-population variation in female preference and correlated variation in male coloration, (ii) differences in how predators versus conspecifics view males, (iii) biased assessment of pigmentary versus structural coloration, (iv) the importance of accounting for multi-species predator communities, and (v) the importance of considering the multivariate genetic architecture and multivariate context of selection and how sexual selection encourages polymorphic divergence. We elaborate these issues using two challenging papers. Our purpose is not to criticize but to point out the potential pitfalls in colour research and to emphasize the depth of consideration necessary for testing evolutionary hypotheses using complex multi-trait phenotypes such as guppy colour patterns.

Selection on sperm size in response to promiscuity and variation in female sperm storage organs.

Sperm cells are exceptionally morphologically diverse across taxa. However, morphology can be quite uniform within species, particularly for species where females copulate with many males per reproductive bout. Strong sexual selection in these promiscuous species is widely hypothesized to reduce intraspecific sperm variation. Conversely, we hypothesize that intraspecific sperm size variation may be maintained by high among-female variation in the size of sperm storage organs, assuming that paternity success improves when sperm are compatible in size with the sperm storage organ. We use individual-based simulations and an analytical model to evaluate how selection on sperm size depends on promiscuity level and variation in sperm storage organ size (hereafter, female preference variation). Simulations of high promiscuity (10 mates per female) showed stabilizing selection on sperm when female preference variation was low, and disruptive selection when female preference variation was high, consistent with the analytical model results. With low promiscuity (2-3 mates per female), selection on sperm was stabilizing for all levels of female preference variation in the simulations, contrasting with the analytical model. Promiscuity level, or mate sampling, thus has a strong impact on the selection resulting from female preferences. Furthermore, when promiscuity is low, disruptive selection on male traits will occur under much more limited circumstances (i.e. only with higher among-female variation) than many previous models suggest. Variation in female sperm storage organs likely has strong implications for intraspecific sperm variation in highly promiscuous species, but likely does not explain differences in intraspecific sperm variation for less promiscuous taxa.

Female Preference for Males Varies with Resource Availability for Reproduction in the Freshwater Goby Tridentiger brevispinis.

Animals with resource-based breeding systems show varying sexual selection modes driven by resource availability. Males of the freshwater goby Tridentiger brevispinis (Pisces: Gobiidae), which are larger, with a longer dorsal-fin, than females, make nests under stones, and provide exclusive parental care of eggs in the nests. For this goby, the nest sites are crucial resources for reproduction. Laboratory experiments that controlled for nest-site abundance were conducted to investigate the effects of nest-site availability on male-male competition and female mate choice. Nest-holding males were on average larger than the average size of all males combined under conditions of low nest-site availability. This result indicates a greater advantage for large males in intrasexual competition for nest sites under conditions of low nest-site availability. Furthermore, egg-guarding males under conditions of low nest-site availability were larger than nest-holding males without eggs. Under conditions of high nest-site availability, the dorsal-fin length of nest-holding males with eggs were longer than those without eggs. These findings suggest that female preference for mates varies qualitatively with nest-site availability. This variation in female preference might result from mate availability that depends upon nest-site availability. The current study concludes that in nest-spawning fishes, nest-site availability can affect the intensity of male-male competition and cause variations of female preference for mates.

Deterring predator pursuit and attracting potential mates? The conspicuous melanized tail display of the zebra-tailed lizard

The evolutionary significance of color expression in animals is often framed within either an interspecific (e.g., antipredator display) or intraspecific (e.g., mate choice) context. In part, this dichotomy stems from assumptions that the expression of conspicuous sexually selected traits likely hinders survival in the wild. Here we address the potential for natural and sexual selection to reinforce expression of a conspicuous tail bar pattern in zebra-tailed lizards (Callisaurus draconoides). In C. draconoides, display of this tail bar pattern has historically been considered an interspecific signal to deter predator pursuit. However, a putative honest link between the tail bar pattern and escape likelihood (e.g., sprint speed) is unknown. Further, studies on related taxa also support the potential for this trait to be informative as a signal of individual quality during mating interactions as well. We assessed variation in the morphology of male and female C. draconoides, and then evaluated how variation in morphology (emphasizing the tail bar pattern) contributed to variation in performance (sprint capacity) and, for males, variation in female preference. Males were larger than females, but size was unrelated to variation in tail bar number. Males sprinted faster than females overall, but tail bar number only mattered for males: specifically, males with more tail bars sprinted faster. Females also preferred males with more tail bars. Overall, our findings suggest that natural (mediated via an honest link between bar number and sprint speed) and sexual (mediated via a preference for males with more tail bars) selection may mutually reinforce expression of a color signal. Thus, the potential adaptive benefits of a color signal may span intra- and interspecific contexts. For males at least, the tail bar pattern is useful for both deterring the pursuit of predators as well as attracting the attention of potential mates.

Strong spatial population structure shapes the temporal coevolutionary dynamics of costly female preference and male display

Female mating preferences for exaggerated male display traits are commonplace. Yet, comprehensive understanding of the evolution and persistence of costly female preference through indirect (Fisherian) selection in finite populations requires some explanation for the persistence of additive genetic variance (V a) underlying sexual traits, given that directional preference is expected to deplete V a in display and hence halt preference evolution. However, the degree to which V a, and hence preference‐display coevolution, may be prolonged by spatially variable sexual selection arising solely from limited gene flow and genetic drift within spatially structured populations has not been examined. Our genetically and spatially explicit model shows that spatial population structure arising in an ecologically homogeneous environment can facilitate evolution and long‐term persistence of costly preference given small subpopulations and low dispersal probabilities. Here, genetic drift initially creates spatial variation in female preference, leading to persistence of V a in display through “migration‐bias” of genotypes maladapted to emerging local sexual selection, thus fueling coevolution of costly preference and display. However, costs of sexual selection increased the probability of subpopulation extinction, limiting persistence of high preference‐display genotypes. Understanding long‐term dynamics of sexual selection systems therefore requires joint consideration of coevolution of sexual traits and metapopulation dynamics.

Female preference for artificial song dialects in the zebra finch (Taeniopygia guttata)

AbstractBirdsong is culturally transmitted, and geographical variations of song have been found in several songbird species. There is evidence that such dialects contribute to reproductive isolation through variation in female preference. In the wild, there is no report of consistent dialects in populations of zebra finches. However, under laboratory conditions, we were able to artificially create different colony‐wide song dialects. In this species, song plays a crucial role in mate choice and the importance of both subadult and adult song experience in shaping song preferences has been well documented. Therefore, we expected females to prefer songs corresponding to their colony's dialect. We measured this preference using an operant test: females could either trigger a song corresponding to their Colony Song Type (CST) sang by an unfamiliar individual, or another conspecific song, corresponding to a Non‐Colony Song Type (N‐CST). Most females preferred the CST over the N‐CST, supporting the idea that zebra finch females exhibit a preference for songs similar to their colony's song. It also reveals that song dialects matter to female zebra finches. It has been proposed that song could be used as an affiliative signal in highly social species. Therefore, preferring the colony dialect could be the consequence of a sexual preference, but also of a social preference. We discuss the potential role of song dialects in the context of social learning.

Within‐population variation in female mating preference affects the opportunity for sexual selection and the evolution of male traits, but things are not as simple as expected

Females from the same population usually have phenotypic variation in their mating preferences. However, the effects of this within-population variation on the sexual selection acting on males are still unclear. We used individual-based models to explore how within-population variation in female preference (i.e. which male trait value is preferred) and preference strength (i.e. how strong the preference is) affects the opportunity for sexual selection (Is ) and the evolution of a sexually selected male trait. We found the highest Is values when females had high variation in preference and an open-ended preference function. The lowest Is occurred when the magnitude of variation in female preference and male trait value were the same and preference function was closed. Male trait exaggeration was higher when there was high within-population variation in preference and females had an open-ended preference function. Also, higher male trait variation was maintained by high variation in preference, but only for a closed preference function. Thus, we found that only within-population variation in female preference, not in preference strength, influences the opportunity for sexual selection and the evolution of sexually selected male traits. Moreover, we found that the shape of the preference function (i.e. open-ended or closed) and the magnitude of within-population variation in female preference compared to male trait variation also influences the Is and consequently the evolution of male traits.

Individual preference functions exist without overall preference in a tropical jumping spider

Female mate choice is a widespread and well-recognized phenomenon. Nevertheless, individual variation in female preference has not yet received the same attention, although such preferences can have important effects on evolutionary dynamics. Here we assess and compare population- and individual-level female preferences for male ornaments and size in the tropical jumping spider Hasarius adansoni in two sets of laboratory experiments. First, we paired females with a single male and quantified receptive behaviours (e.g. receptive posture, number of copulations) and unreceptive behaviours (e.g. attacking the male, running away from a male). We assessed whether these male traits were related to offspring quality and quantity to determine whether there was selection on female preferences. Then, we paired different females with three different-sized males, one per day, and scored similar behaviours to measure preference functions (relationship between male traits and female receptivity). Generally, the population of females did not show a consistent average preference for male traits, despite our finding that females mated to larger males produced more offspring. However, at the individual level, females showed different preference functions for male size, such that some females preferred larger males, while others preferred smaller males. We discuss these data in terms of the causes and consequences of individual preference functions, highlighting the importance of including individual preference functions in future studies that focus on sexual selection and how individual preference can maintain phenotypic variation in wild populations.

Do replicates of independent guppy lineages evolve similarly in a predator-free laboratory environment?

The Trinidadian guppy is emblematic of parallel and convergent evolution, with repeated demonstrations that predation regime is a driver of adaptive trait evolution. A classic and foundational experiment in this system was conducted by John Endler 40 years ago, where male guppies placed into low‐predation environments in the laboratory evolved increased color in a few generations. However, Endler's experiment did not employ the now typical design for a parallel/convergent evolution study, which would employ replicates of different ancestral lineages. We therefore implemented an experiment that seeded replicate mesocosms with small founding populations of guppies originating from high‐predation populations of two very different lineages. The different mesocosms were maintained identically, and male guppy color was quantified every four months. After one year, we tested whether male color had increased, whether replicates within a lineage had parallel phenotypic trajectories, and whether the different lineages converged on a common phenotype. Results showed that male guppy color generally increased through time, primarily due to changes in melanic color, whereas the other colors showed inconsistent and highly variable trajectories. Most of the nonparallelism in phenotypic trajectories was among mesocosms containing different lineages. In addition to this mixture of parallelism and nonparallelism, convergence was not evident in that the variance in color among the mesocosms actually increased through time. We suggest that our results reflect the potential importance of high variation in female preference and stochastic processes such as drift and founder effects, both of which could be important in nature.

Frequency-dependent selection and fluctuations around an equilibrium for alternative reproductive tactics in a swordtail

Negative frequency-dependent selection (NFDS) should have an important role at maintaining equal fitness among different alternative reproductive tactics (ARTs) at an evolutionarily stable state (i.e. equilibrium). Empirical evidence to support both NFDS and equal fitness in the same system is limited. Using the swordtail fish Xiphophorus multilineatus we examined the hypotheses that NFDS may play an important role in maintaining the genetically influenced ARTs in this species at equal fitness. With a mesocosm study we found that sneaker males had a significantly lower reproductive success when they were more common, as expected. Field estimates of relative reproductive success also supported NFDS: the reproductive success of each tactic decreased when they were more common. We then used the field estimates of relative reproductive success and age to sexual maturity in a modified version of the Euler equation to determine whether the relative fitness of the two ARTs was equal in two different periods. Our analysis incorporated both the zero class of males and the invisible fraction, which are often missing from studies of the maintenance of polymorphisms. We found that the population was not at equilibrium during one sample (sneaker frequency 86%) but was at equilibrium during another (sneaker frequency 38%). We discuss factors that may be driving the fluctuations around the equilibrium, including variation in female preferences for courter males, while NFDS may be producing a stable limit cycle around it.

Testing a key assumption in animal communication: between-individual variation in female visual systems alters perception of male signals.

ABSTRACTVariation in male signal production has been extensively studied because of its relevance to animal communication and sexual selection. Although we now know much about the mechanisms that can lead to variation between males in the properties of their signals, there is still a general assumption that there is little variation in terms of how females process these male signals. Variation between females in signal processing may lead to variation between females in how they rank individual males, meaning that one single signal may not be universally attractive to all females. We tested this assumption in a group of female wild-caught brown-headed cowbirds (Molothrus ater), a species that uses a male visual signal (e.g. a wingspread display) to make its mate-choice decisions. We found that females varied in two key parameters of their visual sensory systems related to chromatic and achromatic vision: cone densities (both total and proportions) and cone oil droplet absorbance. Using visual chromatic and achromatic contrast modeling, we then found that this between-individual variation in visual physiology leads to significant between-individual differences in how females perceive chromatic and achromatic male signals. These differences may lead to variation in female preferences for male visual signals, which would provide a potential mechanism for explaining individual differences in mate-choice behavior.

Changes in Mate Preferences by Female Guppies: Effects of Male Phenotypes and Female Age.

In recent decades, variation in female preferences within a species has attracted considerable attention. However, how female individuals in most species change their mate preferences remain unclear. In this study, we examined the change in mate preferences in female individuals of the guppy, Poecilia reticulata. This was done by exposing naïve, virgin females to two male groups differing in the abundance of ornamented males over a period of seven days. The male-exposure treatment groups consisted of (1) primarily males with large orange spots and (2) primarily males with small orange spots. Following each treatment, we measured female preference for brightly colored males with large orange spots, using a pair of digitally modified male images differing in orange spot patterns. Our results indicated that the patterns of change in mate preferences differed between young and old females. After exposure to primarily males with large orange spots, young females were more attracted to the male images overall and showed a preference for the bright male image. Specifically, young females showed a stronger preference for the bright male image when they had been exposed to male groups in which the among-male difference in orange spot patterns was greater. However, in old females, both male-exposure treatments and order of the treatments affected their mate preferences. These results suggest that social components, i.e., both the abundance of ornamented males and the age structure of females in a population, influence the direction and intensity of sexual selection.

Geographical variation in male territory defence strategies in an avian ring species

Interactions between sexual selection and ecology can drive phenotypic divergence between populations. Geographical variation in female preferences has been linked to ecology in several studies, but much less is known about patterns of geographical variation in male competition. I asked whether male aggressive territorial behaviour varied among three breeding populations of a ring species, the greenish warbler, Phylloscopus trochiloides. I measured aggressive response to playbacks of conspecific song at multiple time points to determine how territorial behaviour varied throughout the breeding season both within and between populations. Differences in the abundance and timing of resources necessary for raising offspring can shape male competitive strategies, and competition may consequently vary as a function of resource availability. I therefore combined assays of temporal variation in aggressive behaviour with season-long measures of food abundance, population density and parental provisioning rates. I found that the populations differed in intensity of aggressive response, the seasonal pattern of territoriality and the traits used in territorial responses. Overall intensity of aggression was lowest but most prolonged in the population with the lowest food abundance and highest population density, and males responded to playback primarily by singing. By contrast, birds in the two populations that experienced high food abundance and low population density exhibited a burst of aggressive display behaviour only when females were fertile. The results suggest that territorial strategies vary geographically and respond to limited resources, switching in function from season-long food defence where food is scarce to mate guarding where mates are scarce. Interactions between sexual selection and ecology across large geographical scales may ultimately lead to population divergence. The geographical variation in territorial behaviour observed in the greenish warbler implies that male competition may be an important diversifying force in this system.

Predation Risk Reduces a Female Preference for Heterospecific Males in the Green Swordtail

AbstractThe presence of a predator can result in the alteration, loss or reversal of a mating preference. Under predation risk, females often change their initial preference for conspicuous males, favouring less flashy males to reduce the risk of being detected by predators. Previous studies on predator‐induced plasticity in mate preferences have given females a choice between more and less conspicuous conspecific males. However, in species that naturally hybridize, it is also possible that females might choose an inconspicuous heterospecific male over a conspicuous conspecific male under predation risk. Our study addresses this question using the green swordtail (Xiphophorus helleri) and the southern platyfish (Xiphophorus maculatus), which are sympatric in the wild. We hypothesized that X. helleri females would prefer the sworded conspecific males in the absence of a predator but favour the less conspicuous, swordless, heterospecific males in the presence of a predator. Contrary to our expectation, females associated more with the heterospecific male than the conspecific male in the control (no predator) treatment, and they were non‐choosy in the predator treatment. This might reflect that females were attracted to the novel male phenotype when there was no risk of predation but became more neophobic after predator exposure. Regardless of the underlying mechanism, our results suggest that predation pressure may affect female preferences for conspecific versus heterospecific males. We also found striking within‐population, between‐individual variation in behavioural plasticity: females differed in the strength and direction of their preferences, as well as in the extent to which they altered their preferences in response to changes in perceived predation risk. Such variation in female preferences for heterospecific males could potentially lead to temporal and spatial variation in hybridization rates in the wild.

Does competitive interaction drive species recognition in a house mouse secondary contact zone?

Miscommunication may induce a high risk of unnecessary escalated fights between competitors (populations to species), resulting in selection favoring signal divergence through agonistic character displacement (ACD). When signals allowing discrimination between competitors are also involved in mate recognition, ACD could explain reproductive character displacement (RCD). We tested interference competition between males as a potential driver of RCD (here, subspecies recognition) in a secondary contact zone between two mouse subspecies (Mus musculus musculus and Mus musculus domesticus) displaying asymmetric dominance. Since such asymmetry could create a conflict between subspecies (compatibility) and quality (dominance) recognition in the contact zone, we tested for geographic variation in female preference for dominant males in the subordinate subspecies, musculus. We assessed competition between males and tested ACD during dyadic encounters comparing behavior displayed during trials between heterosubspecifics originating from populations close to the secondary contact (“contact”) and further away (“allopatric”). We also compared behavior of contact versus allopatric males during homosubspecific versus heterosubspecific trials to test whether subspecies discrimination evolved under competitive interference. Although domesticus dominated most heterosubspecific trials regardless of geographic origin, agonistic behavior was more marked (i.e., lower attack latencies) during contact than allopatric encounters, suggesting that ACD occurred. Comparing behavior during homosubspecific and heterosubspecific encounters, only allopatric musculus displayed differences, that is, higher attack latencies toward heterosubspecifics, indicating that discrimination between competitors did not evolve with ACD. Finally, although allopatric musculus females seemed to prefer dominant males, their contact counterparts did not, suggesting that “compatibility” may have outweighed “quality” under a risk of hybridization.

Female preference functions drive interpopulation divergence in male signalling: call diversity in the bushcricket Ephippiger diurnus.

Female preferences play a major role in the elaboration and diversification of male traits: as a selective pressure on males, variation in female preferences can generate population divergence and ultimately, speciation. We studied how interpopulation differences in the shape of female mate preference functions may have shaped male advertisement signals in the bushcricket Ephippiger diurnus. This species is distributed as geographically isolated populations with striking interpopulation variation in male acoustic signals, most notably in the number of syllables per call. Here, we asked whether differences in the shape of preference functions exist among populations and whether those differences may have driven male signal evolution resulting in the observed differences in syllable numbers. Our results reveal fundamental differences in female preferences among populations, with differences in the overall preference function shape corresponding to differences in male signals. These differences in female preferences best explain the major differences in male signals among populations. The interpopulation variation in signals and preferences potentially reflects the evolutionary history of the species and may contribute to further divergence among populations and subsequent speciation.

Male–female genotype interactions maintain variation in traits important for sexual interactions and reproductive isolation

Prezygotic reproductive isolation can evolve quickly when sexual selection drives divergence in traits important for sexual interactions between populations. It has been hypothesized that standing variation for male/female traits and preferences facilitates this rapid evolution and that variation in these traits is maintained by male-female genotype interactions in which specific female genotypes prefer specific male traits. This hypothesis can also explain patterns of speciation when ecological divergence is lacking, but this remains untested because it requires information about sexual interactions in ancestral lineages. Using a set of ancestral genotypes that previously had been identified as evolving reproductive isolation, we specifically asked whether there is segregating variation in female preference and whether segregating variation in sexual interactions is a product of male-female genotype interactions. Our results provide evidence for segregating variation in female preference and further that male-female genotype interactions are important for maintaining variation that selection can act on and that can lead to reproductive isolation.

Variation in social relationships relates to song preferences and EGR1 expression in a female songbird.

Social experiences can profoundly shape social behavior and the underlying neural circuits. Across species, the formation of enduring social relationships is associated with both neural and behavioral changes. However, it remains unclear how longer-term relationships between individuals influence brain and behavior. Here, we investigated how variation in social relationships relates to variation in female preferences for and neural responses to song in a pair-bonding songbird. We assessed variation in the interactions between individuals in male-female zebra finch pairs and found that female preferences for their mate's song were correlated with the degree of affiliation and amount of socially modulated singing, but not with the frequency of aggressive interactions. Moreover, variation in measures of pair quality and preference correlated with variation in the song-induced expression of EGR1, an immediate early gene related to neural activity and plasticity, in brain regions important for auditory processing and social behavior. For example, females with weaker preferences for their mate's song had greater EGR1 expression in the nucleus Taeniae, the avian homologue of the mammalian medial amygdala, in response to playback of their mate's courtship song. Our data indicate that the quality of social interactions within pairs relates to variation in song preferences and neural responses to ethologically relevant stimuli and lend insight into neural circuits sensitive to social information. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1029-1040, 2016.

Phylogenetic Correlation Between Male Nuptial Color and Behavioral Responses to Color Across a Diverse and Colorful Genus of Freshwater Fish (Etheostoma spp., Teleostei: Percidae)

AbstractSexual selection theory predicts that preferences in both sexes select for the elaboration of male nuptial coloration, with empirical evidence supporting these predictions. Empirical studies are often limited in their taxonomic inclusiveness, however, and typically do not examine how male and female preferences contribute to macroevolutionary patterns of male color variation across multiple lineages in a clade. This study examined color preferences in a group of dichromatic freshwater fishes known as darters (genus Etheostoma) that vary in the presence of male coloration. The strengths of attraction to black, blue, gray, and red models were tested in females of 18 species, in addition to males of five species. We found a positive association between the presence of red or orange on the body and the amount of time associating with red models, suggesting color variation is at least in part due to variation in female preferences between species. Males also spent more time associating with colors that most closely resembled conspecifics, suggesting that preferential responses to color in males also can contribute to the diversity of nuptial coloration in darters.

Social experience affects female mate preferences for a visual trait in a wolf spider

Females often prefer males with bright, showy, or large secondary sexual characters. However, social experience can result in variation in female preferences, with evidence of sexual imprinting in some taxa. In the brush-legged wolf spider, Schizocosa ocreata, asynchrony of maturation provides a time period in which imprinting may occur. We tested whether adult females demonstrated plasticity in their visual preferences for male leg tuft size after experience with digitally courting males during their penultimate stage. Penultimate instar females were presented visual courtship signals from males with small, average, or large tufts; a mixture of tuft sizes; or no males at all. During Week 2 of adulthood, each female was presented playback of digital courting small- and/or large-tufted males in both no-choice and two-choice presentations. Adult female preferences varied significantly with prior experience. Females exposed to only large-tufted males or males with a mixture of tuft sizes demonstrated more receptivity displays to large-tufted males than small-tufted males. Females exposed to only small-tufted males demonstrated more receptivity displays toward small-tufted males than large-tufted males. Because results suggested the possibility of sexual imprinting, we tested for reversibility. A subset of females was retested for selectivity in two-choice trials, revealing a positive correlation between Week 2 and Week 5 female selectivity. Females previously exposed to small-tufted males, however, no longer maintained their preference for small-tufted males in Week 5. This study demonstrates the effects of an individual’s social environment on mating preferences, and the importance of age and timing when studying sexual imprinting.