Hybrid female mate choice as a species isolating mechanism: environment matters

A fundamental goal of biology is to understand how new species arise and are maintained. Female mate choice is potentially critical to the speciation process: mate choice can prevent hybridization and thereby generate reproductive isolation between potentially interbreeding groups. Yet, in systems where hybridization occurs, mate choice by hybrid females might also play a key role in reproductive isolation by affecting hybrid fitness and contributing to patterns of gene flow between species. We evaluated whether hybrid mate choice behaviour could serve as such an isolating mechanism using spadefoot toad hybrids of Spea multiplicata and Spea bombifrons. We assessed the mate preferences of female hybrid spadefoot toads for sterile hybrid males vs. pure‐species males in two alternative habitat types in which spadefoots breed: deep or shallow water. We found that, in deep water, hybrid females preferred the calls of sterile hybrid males to those of S. multiplicata males. Thus, maladaptive hybrid mate preferences could serve as an isolating mechanism. However, in shallow water, the preference for hybrid male calls was not expressed. Moreover, hybrid females did not prefer hybrid calls to those of S. bombifrons in either environment. Because hybrid female mate choice was context‐dependent, its efficacy as a reproductive isolating mechanism will depend on both the environment in which females choose their mates as well as the relative frequencies of males in a given population. Thus, reproductive isolation between species, as well as habitat specific patterns of gene flow between species, might depend critically on the nature of hybrid mate preferences and the way in which they vary across environments.     

Repeatability of mate choice in female red jungle fowl

We staged female mate choice trials between pairs of males andrepeated the process for each female to determine the repeatabilityof female preference for males in red jungle fowl (Gallus gallus)in the first and second half of the breeding season. We measuredmale morphological traits (the size and color of the comb andthe brightness of the hackle feathers) that females are knownto use in choosing a mate. In the first half of the breedingseason, females showed repeatability in their choices of matewith respect to the male's comb characters. Females did notshow a repeatable preference with respect to male hackle feathers,and we found no repeatability of mate choice in the second halfof the season. Females seem to primarily look at the male'scomb when choosing a mate, and other ornaments seem only ofsecondary importance.[Behav Ecol 7: 243-246 (1996)]     

Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis

Sexual selection theory asserts that females are well adapted to sense signals indicating the quality of potential mates. One crucial male quality parameter is functional fertility (i.e. the success of ejaculates in fertilizing eggs). The phenotype-linked fertility hypothesis (PLFH) predicts that functional fertility of males is reflected by phenotypic traits that influence female mate choice. Here, we show for Nasonia vitripennis, a parasitic wasp with haplodiploid sex determination and female-biased sex ratios, that females use olfactory cues to discriminate against sperm-limited males. We found sperm limitation in newly emerged and multiply mated males (seven or more previous matings) as indicated by a higher proportion of sons in the offspring fathered by these males. Sperm limitation correlated with clearly reduced pheromone titres. In behavioural bioassays, females oriented towards higher doses of the synthetic pheromone and were attracted more often to scent marks of males with a full sperm load than to those of sperm-limited males. Our data support the PLFH and suggest that N. vitripennis females are able to decrease the risk of getting constrained to produce suboptimal offspring sex ratios by orienting towards gradients of the male sex pheromone.     

Liking the good guys: amplifying local adaptation via the evolution of condition‐dependent mate choice

Local adaptation can be strengthened through a diversity of mechanisms that reduce gene flow between contrasting environments. Recent work revealed that mate choice could enhance local adaptation when females preferentially mate with locally adapted males and that such female preferences readily evolve, but the opposing effects of recombination, migration and costs of female preferences remain relatively unexplored. To investigate these effects, we develop a two‐patch model with two genes, one influencing an ecological trait and one influencing female preferences, where both male signals and female preferences are allowed to depend on the match between an individual's ecological trait and the local environment (condition). Because trait variation is limited when migration is rare and the benefits of preferential mating are short‐lived when migration is frequent, we find that female preferences for males in high condition spread most rapidly with intermediate levels of migration. Surprisingly, we find that preferences for locally adapted males spread fastest with higher recombination rates, which contrasts with earlier studies. This is because a stronger preference allele for locally adapted males can only get uncoupled from maladapted ecological alleles following migration through recombination. The effects of migration and recombination depend strongly on the condition of the males being chosen by females, but only weakly on the condition of the females doing the choosing, except when it comes to the costs of preference. Although costs always impede the spread of female preferences for locally adapted males, the impact is substantially lessened if costs are borne primarily by females in poor condition. The abundance of empirical examples of condition‐dependent mate choice combined with our theoretical results suggests that the evolution of mate choice could commonly facilitate local adaptation in nature.     

A theory of mate choice based on heterozygosity

In theories of mate choice that rely on genetic benefits, thenature of the"good genes" involved has received little attention.A review of genetic studies of mate choice in a variety of speciesand situations suggests that individual heterozygosity is moreimportant than previously realized. Females are predicted tovalue heterozygosity in their offspring and under some conditionsin their males. The expression of vigor, condition-sensitiveornaments, and symmetry in males may be a direct reflectionnot of "good genes" but of individual heterozygosity at keyloci or at many loci. Like sexuality itself, mate choice basedon heterozygosity and genic diversity may be an adaptation thatfavors the production of diverse and superior competitors. Femalechoice is made meaningful by sexuality, and the adaptive valueof choice probably depends on some of the same factors thatmaintain sexuality     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

No female mate choice in Mallee dragon lizards, Ctenophorus fordi

Aspects of sexual selection were studied in a sexually monomorphic Australian agamid lizard (Ctenophorus fordi), in particular with respect to the sensory exploitation hypothesis. In enclosure trials, females were offered the choice between large vs. small males and, in a different experiment, males with blue vs. normal head color. The rationale for these experiments was: firstly, to establish if females actively solicit copulations; secondly, if so, do females solicit copulations non-randomly with respect to male size (because large males may have access to food resources); thirdly, if male coloration is manipulated to match traits of congeneric, conspicuous and sexually dimorphic species, do females show preference for this novel trait (in accordance with the sensory exploitation hypothesis). The corresponding manipulations were also made in a free-living population where the distribution of females on the home ranges of color-manipulated males were monitored. Blue-headed males were accepted as mating partners both in the staged mating trials and in the natural population. Females appeared not to express any kind of active or passive mate choice (rejection); in only one out of 62 trials did a female approach a male herself rather than being approached by the male(s). There was no discrimination against any male category regardless of size or color within a female's receptive period and the manipulation of male head color in the natural population did not result in spatial re-distribution of females. Thus, a female appears to mate unselectively within her receptive period. Rejection behaviors were used only outside of the receptive period to communicate, to all males, that the female is not receptive.     

Female mate choice across mating stages and between sequential mates in flour beetles

Few studies have examined how female premating choice correlates with the outcome of copulatory and post-copulatory processes. It has been shown that polyandrous Tribolium castaneum females discriminate among males before mating based on olfactory cues, and also exert cryptic choice during mating through several mechanisms. This study tested whether a male's relative attractiveness predicted his insemination success during copulation. Bioassays with male olfactory cues were used to rank two males as more and less attractive to females; each female was then mated to either her more attractive male followed by less attractive male, or vice versa. Dissections immediately after second copulations revealed a significantly higher percent of successful inseminations for females that remated with more attractive males compared with those that remated with less attractive males. These results indicate that cryptic female choice during copulation reinforces precopulatory female choice in T. castaneum, and suggest that females could use cryptic choice to trade up to more attractive males, possibly gaining better phenotypic or genetic quality of sires.     

Character displacement and the evolution of mate choice: an artificial neural network approach

Interactions with heterospecifics can promote the evolution of divergent mating behaviours between populations that do and do not occur with heterospecifics. This process--reproductive character displacement--potentially results from selection to minimize the risk of mating with heterospecifics. We sought to determine whether heterospecific interactions lead to divergence of female preferences for aspects of conspecific male signals. We used artificial neural network models to simulate a mate recognition system in which females co-occur with different heterospecifics in different populations. Populations that evolved conspecific recognition in the presence of different heterospecifics varied in their preferences for aspects of conspecific male signals. When we tested networks for their preferences of conspecific versus heterospecific signals, however, we found that networks from allopatric populations were usually able to select against heterospecifics. We suggest that female preferences for aspects of conspecific male signals can result in a concomitant reduction in the likelihood that females will mate with heterospecifics. Consequently, even females in allopatry may discriminate against heterospecific mates depending on the nature of their preferences for conspecifics. Such a pattern could potentially explain cases where reproductive character displacement is expected, but not observed.     

Genes, copying, and female mate choice: shifting thresholds

Recent experimental work on guppies (Poecilia reticulata) hasexamined the strength of genetic and cultural (copying) factorsin determining female mate choice. Using females from a populationwith a heritable preference for the amount of orange body colorpossessed by males, prior work discovered that a threshold differencein orange color among males existed below which females wouldchoose a less orange male if they observed another female choosethat male, but above which they consistently preferred the moreorange of the males, regardless of whether they viewed anotherfemale prefer the less orange male. I tested whether this thresholdcan be shifted by increasing the amount of mate-copying informationavailable to a female. I demonstrate that when a female hasthe opportunity to see two different model females independentlyprefer the less orange of two males or a single female neara drab male for a longer period of time (twice as long as inprior work), the observer female prefers this drab male evenwhen males dramatically differ in orange coloration.     

Prior exposure to male phenotypes influences mate choice in the guppy, Poecilia reticulata

This study examined the effect of experience on the patternof mate choice in female guppies. Females from some naturalpopulations are known to discriminate among males on the basisof the relative area of orange in the color pattern. We exposedmaturing female guppies to groups of males that differed inphenotvpic distribution of orange coloration (high orange, loworange, and mixed) and tested their subsequent mating preferences.Females that had been exposed to high-orange or low-orange malegroups showed no discrimination in choice tests, but femalesexposed to mixed male groups favored high-orange males overlow-orange males. These results demonstrate that mating preferencesof females can be modified depending on prior experience. Femalesmay be able to adjust their pattern of mate choice dependingon the degree to which choice cues permit effective discriminationamong males. This potential for short-term modification of matechoice patterns could affect the evolutionary outcome of sexualselection     

Environment-dependent selection on mate choice in a natural population of birds

Female mate choice acts as an important evolutionary force, yet the influence of the environment on both its expression and the selective pressures acting upon it remains unknown. We found consistent heritable differences between females in their choice of mate based on ornament size during a 25-year study of a population of collared flycatchers. However, the fitness consequences of mate choice were dependent on environmental conditions experienced whilst breeding. Females breeding with highly ornamented males experienced high relative fitness during dry summer conditions, but low relative fitness during wetter years. Our results imply that sexual selection within a population can be highly variable and dependent upon the prevailing weather conditions experienced by individuals.     

Direct mate choice maintains diversity among sympatric cichlids in Lake Victoria

Mate choice may play an important role in animal speciation. The haplochromine cichlids of Lake Victoria are suitable to test this hypothesis. Diversity in ecology, coloration and anatomy evolved in these fish faster than postzygotic barriers to gene flow, and little is known about how this diversity is maintained. It was tested whether recognizable forms are selection-maintained morphs or reproductively isolated species by investigating in the field reproductive timing, location of spawning sites, and mate choice behaviour. There was a large interspecific overlap in timing of breeding and location of spawning sites, which was largest in members of the same genus. Behavioural mate choice of such closely related taxa was highly assortative, such that it is likely that they are sexually isolated species and that direct mate choice is the major force that directs gene flow and maintains form diversity. The results differ from what is known about recent radiations of other lacustrine fish groups where speciation seems to be driven by diverging microhabitat preferences or diverging timing of reproduction, but are in agreement with predictions from models of speciation by diverging mate preferences.     

Reinforcement shapes clines in female mate discrimination in Drosophila subquinaria

Reinforcement of species boundaries may alter mate recognition in a way that also affects patterns of mate preference among conspecific populations. In the fly Drosophila subquinaria, females sympatric with the closely related species D. recens reject mating with heterospecific males as well as with conspecific males from allopatric populations. Here, we assess geographic variation in behavioral isolation within and among populations of D. subquinaria and use cline theory to understand patterns of selection on reinforced discrimination and its consequences for sexual isolation within species. We find that selection has fixed rejection of D. recens males in sympatry, while significant genetic variation in this behavior occurs within allopatric populations. In conspecific matings sexual isolation is also asymmetric and stronger in populations that are sympatric with D. recens. The clines in behavioral discrimination within and between species are similar in shape and are maintained by strong selection in the face of gene flow, and we show that some of their genetic basis may be either shared or linked. Thus, while reinforcement can drive extremely strong phenotypic divergence, the long‐term consequences for incipient speciation depend on gene flow, genetic linkage of discrimination traits, and the cost of these behaviors in allopatry.     

The evolution of male mate choice in insects: a synthesis of ideas and evidence

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.     

The empirical question of thresholds and mechanisms of mate choice

Summary Theoretical discussions concerning how animals might best sample and select mates have suggested that individuals could base decisions either on a sample of mates (sampled-based decisions) or on a threshold of comparison (threshold-based decisions). Recent theoretical work demonstrates that threshold-based mating decisions generate higher expected fitness than sample-based mating decisions when search costs exist. Empirical results from most unmanipulated systems, however, either conclude that females make sample-based decisions or are inconclusive. A few experimental studies designed to detect mating thresholds purport to demonstrate threshold-based choice but an examination of these studies indicates such conclusions were premature. We believe that few examples of threshold-based choice exist because protocols designed to identify mating thresholds were often inconsistent with models of threshold choice. We suggest that future empirical work strive not to document mating thresholdsper se. Rather, future work might best reveal decision rules by manipulating the distribution of quality among potential mates; such manipulations predict uniquely how females using sample-based and threshold-based decision rules should behave.     

Ultraviolet vision and mate choice in the guppy (Poecilia reticulata)

Ultraviolet (UV) vision is well documented for many speciesof vertebrates. UV cues are known to be used in foraging, navigationand in mate choice. We conducted a series of behavioral experimentsto investigate the role of UV perception in mate choice inboth female and male guppies (Poecilia reticulata). In ourexperiments the visual appearance of potential mates was manipulatedusing either UV transmitting (UV+) or UV blocking (UV-) filters.Female guppies significantly preferred UV+ males. Male guppiestended to prefer UV- females, but their preferences were marginallynonsignificant. Further experiments investigating the roleof luminance, indicate that UV wavelengths are probably beingused for color discrimination rather than for detecting differencesin brightness. These experiments raise the possibility thatUV is used in mate assessment in different ways by male andfemale guppies. This may reflect the different strategies thatthe two sexes have in order to maximize reproductive success.To our knowledge, these are the first data showing that UVis used by any fish species in mate selection.