Male courtship preferences demonstrate discrimination against allopatric colour morphs in a cichlid fish

Whether premating isolation is achieved by male‐specific, female‐specific or sex‐independent assortative preferences often depends on the underlying evolutionary processes. Here we test mate preferences of males presented with females of different allopatric colour variants of the cichlid fish Tropheus sp., a Lake Tanganyika endemic with rich geographical colour pattern variation, in which the strength of sexual isolation varies between populations. We conducted two‐way mate choice experiments to compare behaviour of males of a red‐bodied morph (population Moliro) towards females from their own population with behaviour towards females from four allopatric populations at different stages of phylogenetic and phenotypic divergence. Males courted same‐population females significantly more intensely than females of other populations, and reduced their heteromorphic courtship efforts both with increasing genetic and increasing phenotypic distinctness of the females. In particular, females of a closely related red‐bodied population received significantly more courtship than either genetically distinct, similarly coloured females (‘Kirschfleck’ morph) or genetically related, differently coloured females (‘yellow‐blotch’ morph), both of which were courted similarly. Genetically and phenotypically distinct females (Tropheus polli) were not courted at all. Consistent with previous female‐choice experiments, female courtship activity also decreased with increasing genetic distance from the males’ population. Given successful experimental and natural introgression between colour morphs and the pervasive allopatry of related variants, we consider it unlikely that assortative preferences of both sexes were driven by direct selection during periods of secondary contact or, in turn, drove colour pattern differentiation in allopatry. Rather, we suggest that sexual isolation evolved as by‐product of allopatric divergence.     

Sperm Competition in a Viviparous Fish

We investigated multiple paternity and sperm precedence in the Amarillo fish, Girardinichthys multiradiatus (Goodeidae). We allowed females to mate with two different-sized males consecutively and assessed the paternity of the ensuing broods using allozyme electrophoresis. We presented one-half of the females the larger, and the other half the smaller, male first. Allozyme variation among individuals was low, yielding conservative estimates of multiple paternity. Half the broods were of mixed paternity, but one male always sired more than 70% of the embryos in each brood. The proportion of the brood sired was not related to mating sequence, but when we classified males by relative size, the larger male of each pair usually fathered greater proportions of offspring than the smaller male. This association disappeared when we used the actual size of the males in the analysis. Instead, for any pair of males, the difference in number of offspring sired was correlated to differences in the rate of courtship displays, rather than size differences, suggesting that courtship intensity is a better predictor of paternity than male size. Within a pair, the larger male usually displayed more than the smaller one, but there was no correlation between male size and display rate across all males. Parsimony suggests a correlation between courtship rate and sperm production, but we cannot rule out the possibility that females allocate paternity according to the relative merits of the males.     

SIMULATING RANGE EXPANSION: MALE SPECIES RECOGNITION AND LOSS OF PREMATING ISOLATION IN DAMSELFLIES

Prolonged periods of allopatry might result in loss of the ability to discriminate against other formerly sympatric species, and can lead to heterospecific matings and hybridization upon secondary contact. Loss of premating isolation during prolonged allopatry can operate in the opposite direction of reinforcement, but has until now been little explored. We investigated how premating isolation between two closely related damselfly species, Calopteryx splendens and C. virgo , might be affected by the expected future northward range expansion of C. splendens into the allopatric zone of C. virgo in northern Scandinavia. We simulated the expected secondary contact by presenting C. splendens females to C. virgo males in the northern allopatric populations in Finland. Premating isolation toward C. splendens in northern allopatric populations was compared to sympatric populations in southern Finland and southern Sweden. Male courtship responses of C. virgo toward conspecific females showed limited geographic variation, however, courtship attempts toward heterospecific C. splendens females increased significantly from sympatry to allopatry. Our results suggest that allopatric C. virgo males have partly lost their ability to discriminate against heterospecific females. Reduced premating isolation in allopatry might lead to increased heterospecific matings between taxa that are currently expanding and shifting their ranges in response to climate change.     

Subspecies recognition in the house mouse: a study of two populations from the border of a hybrid zone

Mate choice is the outcome of sexual preference for partnerscarrying specific signals. Thus, mating among conspecifics(homogamy) depends on the occurrence of species recognitionsystems. We asked what happens if populations diverge, andwe investigated female sexual preference between two subspeciesof the house mouse in populations from the borders of a hybridzone (Jutland, Denmark). We used choice tests to analyze theoccurrence of recognition signals and to locate these signalsin soiled bedding and urine. Our results show that populationsof the two subspecies can be discriminated on the basis ofurinary signals, suggesting that the latter have diverged. Additionally, these signals seem to have similar features inpopulations of different geographical origins, suggesting thatsubspecific differentiation occurs. This is the first demonstrationthat subspecific recognition through urinary signals occursin the house mouse. However, while Mus musculus domesticusdoes not display a preference, we show that Mus musculus musculusfemales tend to mate with males of the same subspecies. We discuss the different factors that could explain these discrepanciesbetween females of the two taxa: differences in signal perception,evolution at a different pace, or evolution under differentselective pressures in their area of contact. Further, we proposethat the divergence in male signal was at least partly initiatedin allopatry and discuss different evolutionary scenario thatmay explain the patterns observed in Denmark and their relevance to isolation between the two taxa.     

Does courtship behavior contribute to species-level reproductive isolation in field crickets?

Reproductive behavior influences gene flow within and amongspecies; thus, sexual selection may be a major contributor tothe maintenance of species, and possibly their formation. HereI experimentally manipulate the courtship interactions of thefield crickets Gryllus rubens and G. texensis to examine thepotential of close-range courtship interactions to limit interspecificgene flow. Responses of males to females and of females to malecourtship song and males per se were examined for four pairedsympatric and allopatric populations. Male G. rubens were morelikely to court conspecific females, but male G. texensis courtedfemales of both species equally. If paired with conspecificmales, female G. rubens and G. texensis both preferred conspecificcourtship song. In none of these comparisons were the responsesof males or females from allopatry different from those in sympatry.There was an asymmetry of courtship response across both sexand species: male G. rubens were more discriminating than maleG. texensis, whereas female G. texensis were more discriminatingthan female G. rubens. Despite significant preferences for conspecifics,the net effect of courtship interactions would appear to limitinterspecific gene flow only weakly. These results are consistentwith courtship behavior evolving under the influence of sexualselection and only indirectly promoting species integrity.     

Male competition is disruptive to courtship in the Pacific blue‐eye

The present study examined the effects of competition on male courtship in the Pacific blue‐eye Pseudomugil signifer , a species of fish where females have previously been shown to use courtship, but not male fighting prowess, as an important mate choice cue. Courtship bouts directed to a stimulus female were shortest when two males were allowed to freely interact (contact treatment) and longest when there was only one male (non‐interaction). Courtship length in trials where one of two males was confined to a clear cylinder (visual) was intermediate between the other two treatments. Courtship in visual and contact treatments was constantly disrupted. The percentage of interrupted courtships was higher for the contact compared to visual treatment where aggressive interactions were also longer in duration and took place more frequently. Within contact trials, dominant males courted longer than subordinates despite both males experiencing comparable rates of courtship disruption. These results suggest that male‐male competition can have important implications for adaptive female choice particularly in circumstances where the benefits being sought by females are unrelated to male fighting ability.     

Evidence for no sexual isolation between Drosophila albomicans and D. nasuta

Sexual isolation, the reduced tendency to mate, is one of the reproductive barriers that prevent gene flow between different species. Various species‐specific signals during courtship contribute to sexual isolation between species. Drosophila albomicans and D. nasuta are closely related species of the nasuta subgroup within the Drosophila immigrans group and are distributed in allopatry. We analyzed mating behavior and courtship as well as cuticular hydrocarbon profiles within and between species. Here, we report that these two species randomly mated with each other. We did not observe any sexual isolation between species or between strains within species by multiple‐choice tests. Significant difference in the courtship index was detected between these two species, but males and females of both species showed no discrimination against heterospecific partners. Significant quantitative variations in cuticular hydrocarbons between these two species were also found, but the cuticular hydrocarbons appear to play a negligible role in both courtship and sexual isolation between these two species. In contrast to the evident postzygotic isolation, the lack of sexual isolation between these two species suggests that the evolution of premating isolation may lag behind that of the intergenomic incompatibility, which might be driven by intragenomic conflicts.     

Dual Signaling during Mating in Brown-headed Cowbirds (Molothrus ater,Family Emberizidae/Icterinae)

Male brown-headed cowbirds (Molothrus ater) vocalize to females during pair formation, a period usually lasting several days. Males also vocalize to females in the seconds immediately prior to females' adopting copulatory postures. The two major classes of male vocalizations occurring during courtship and copulation are songs and flight whistles. Observations across the species' North American range suggest that the function of these two courtship vocalizations may differ geographically. Aviary observations of eastern and midwestern populations suggested, furthermore, that the precise timing of song and whistle used during copulation sequences differs, with flight whistles occurring most often after a copulatory posture but before the male mounts and the pair copulates. Such timing of the two signals suggested different proximate functions. Here, we report three experiments that addressed the communicative properties of the two signals in two midwestern populations. First, we tested females of the two populations in two playback experiments to determine copulatory responsiveness and discrimination of the two signals. We asked whether females of the two populations gave more copulatory responses to the playbacks of songs and flight whistles of males of their own population than to those of males of the other population, and whether females responded differently to songs than to whistles. In the third experiment, we observed courtship interactions among males and females from one population in a large aviary to assess the use of flight whistles in relation to courtship success. Females of both populations responded more frequently to playbacks of songs than to playbacks of flight whistles and showed reliably more responsiveness to local song variants. Thus, information in male song can be used by females to discriminate the local population. The aviary data revealed that the rate of flight whistling correlated strongly with male courtship success. Thus, the vocal antecedents to mating in midwestern cowbirds include close-range signaling to females followed by longer range signaling, perhaps to other males and to females other than the mate. Acoustic and behavioral differences between these two signals in diverse parts of the cowbirds' range suggest that the function of ‘speciestypical’ signals such as songs or whistles may not be fixed, a conclusion in keeping with the growing evidence of vocal and social mallcability in these brood parasitic birds.     

Amarillo Fish (Girardinichthys multiradiatus) Use Visual Landmarks to Orient in Space

Fish responsiveness to visual stimuli has been studied extensively in contexts such as female mate choice, predator inspection and schooling, yet surprisingly little work has been conducted on visual orientation in space in fish. Here we report on an experiment designed to test whether Amarillo fish can learn to find a goal within a maze more effectively in the presence of local visual landmarks than otherwise. We found that: (a) Amarillo fish can use landmarks to locate a goal, (b) there was no observed difference in the ability to use visual landmarks between two populations and (c) overall navigational performance differed between two populations of Amarillo fish: individuals from a permanently turbid eutrophic pond performed better than those from a pond with clear waters. We hypothesize that fish that inhabit clear waters possess poorer navigational capabilities than fish from turbid waters because they normally rely on goal‐oriented behaviour, which requires neither egocentric nor environmental clues to navigate. This paper adds to the literature on the links between habitat characteristics and population differences in performance.     

Female choice for male motor skills

Sexual selection was proposed by Darwin to explain the evolution of male sexual traits such as ornaments and elaborate courtship displays. Empirical and theoretical studies have traditionally focused on ornaments; the reasons for the evolution of elaborate, acrobatic courtship displays remain unclear. We addressed the hypothesis that females choose males on the basis of subtle differences in display performance, indicating motor skills that facilitate survival. Male golden-collared manakins (Manacus vitellinus) perform elaborate, acrobatic courtship displays. We used high-speed cameras to record the displays of wild males and analysed them in relation to male reproductive success. Females preferred males that performed specific display moves at greater speed, with differences of tens of milliseconds strongly impacting female preference. In additional males, we recorded telemetrically the heart rate during courtship using miniature transmitters and found that courtship is associated with profoundly elevated heart rates, revealing a large metabolic investment. Our study provides evidence that females choose their mates on the basis of subtle differences in motor performance during courtship. We propose that elaborate, acrobatic courtship dances evolve because they reflect motor skills and cardiovascular function of males.     

Individual Variation in Male Size and Behavioral Repertoire in the Sailfin Molly Poecilia latipinna

Variation among individuals in the expression of behaviors and associations of behaviors in different contexts can lead to the maintenance of behavioral polymorphisms. Individual variation in morphology is often associated with behavioral polymorphism, yet the degree to which morphology predicts behavioral phenotype is not well understood. We measured individual variation in size and behaviors in the sailfin molly, Poecilia latipinna, by comparing the behavior of individual males of different sizes across four different contexts (mating, exploratory tendency, sociability, and predator inspection). We also investigated the degree to which male size, a fixed genetic trait, influenced the expression of each behavior and associations between behaviors. We found that male mollies show strong associations between certain behaviors and only some of these are predicted by male size. For example, size has a strong influence on the courtship‐boldness axis with larger males showing higher rates of courtship displays and being bolder in predator inspection. A positive association was found between exploratory tendency, sociability, and gonopodial thrusting rates, yet the expression of these behaviors was independent of male size. Thus, sailfin mollies, like many fish species, show associations of behaviors that contribute to differences among males in personality type. The fixed genetic effect of male size at maturity influences courtship and boldness, but individual variation in exploratory tendency, sociability, and sneak copulation attempts through gonopodial thrusts is independent of male size. Such variation among males in behavioral associations within and between different contexts may slow the rate at which populations of P. latipinna can diverge in individual behaviors.     

Population and Species Divergence of Chemical Cues that Influence Male Recognition of Females in Desmognathine Salamanders

Growing evidence indicates that males may be more discriminating of mating partners than often has been assumed. In the North American Ocoee dusky salamander, Desmognathus ocoee (Plethodontidae: Desmognathinae), sexual incompatibility among conspecific populations is high in encounters staged in the laboratory, at least in part because males fail to recognize ‘other’ females as appropriate targets for courtship. I used Y-mazes to test the hypothesis that males of D. ocoee discriminate between substrate-borne chemical cues produced by ‘own’ (homotypic) and ‘other’ (heterotypic) females. Males of four populations discriminated in favor of substrates soiled by homotypic females over clean (control) substrates (expt 1), suggesting that females produce chemical cues of sociosexual significance to males. Furthermore, males from these populations discriminated in favor of substrates soiled by homotypic females vs. substrates soiled by heterotypic females (expt 2), both conspecific and heterospecific (D. carolinensis and D. orestes). Thus, differences among populations and species in female chemical cues appear to affect the chemotactic responses of males. I suggest that, together with differences in behavioral signals and responses exhibited during courtship, differences in female chemical cues likely contribute to sexual incompatibility among populations and taxa of desmognathine salamanders.     

Female Choice and the Consistency of Courtship Feeding in Black-horned Tree Crickets Oecanthus nigricornis Walker (Orthoptera: Gryllidae: Oecanthinae)

Courtship feeding in insects is often strongly correlated with insemination duration and therefore provides a potential postcopulatory episode of sexual selection. We tested whether courtship feeding and other courtship traits in the black-horned tree cricket Oecanthus nigricornis showed sufficient consistency potentially to respond to sexual selection by testing whether they differed significantly among males. Duration of courtship feeding differed among males when measured repeatedly and this caused significant differences in the duration of spermatophore attachment, a trait that determines the maximum duration of insemination and thus has important fitness consequences in crickets. We also partitioned variance in courtship behaviour between the sexes to test whether differences in courtship behaviour were attributable primarily to males, females or both sexes. Duration of spermatophore attachment was controlled by females and therefore represents a mechanism of female mate choice. Significant variation in duration of spermatophore attachment was associated with differences between individuals of both sexes. Differences among males indicate that females agree in their preference of certain males whereas differences among females indicate that females differ in their receptivity to postcopulatory courtship and insemination. The fact that differences among males in duration of spermatophore attachment were due to significant differences solely in the period of courtship feeding indicates that postcopulatory female choice was mediated through courtship feeding. Whether males manipulate female choices by allocating more or fewer resources requires further testing, but we found that males court some females more vigorously than others after females dismount. The number of previous mates had opposite effects on the duration of courtship feeding for the sexes, decreasing it for males but increasing it for females, and we discuss the possible causes of these results.     

Reproductive character displacement generates reproductive isolation among conspecific populations: an artificial neural network study

When interactions with heterospecifics prevent females from identifying conspecific mates, natural selection can promote the evolution of mating behaviours that minimize such interactions. Consequently, mating behaviours may diverge among conspecific populations in sympatry and in allopatry with heterospecifics. This divergence in conspecific mating behaviours-reproductive character displacement-can initiate speciation if mating behaviours become so divergent as to generate reproductive isolation between sympatric and allopatric conspecifics. We tested these ideas by using artificial neural networks to simulate the evolution of conspecific mate recognition in populations sympatric and allopatric with different heterospecifics. We found that advertisement calls diverged among the different conspecific populations. Consequently, networks strongly preferred calls from their own population to those from foreign conspecific populations. Thus, reproductive character displacement may promote reproductive isolation and, ultimately, speciation among conspecific populations.     

Male Siamese Fighting Fish, Betta splendens, Increase Rather than Conceal Courtship Behavior when a Rival is Present

The impact of social environment on mating success is especially pronounced in species where both intraspecific and interspecific selection influence reproduction, such as the Siamese fighting fish. Males alter male–male interactions when either a male or female audience is present, but how males change their behavior toward a female when a rival male is present is unknown. This study addresses whether males alter their behavior toward a female in a way that would prevent a rival male from interrupting courtship. The behavior of male Siamese fighting fish toward a dummy female was examined under various degrees of visual cover, both in the presence and absence of a rival male, to investigate whether males use concealment provided by the structural environment to their advantage. While males did not use barriers to conceal courtship as hypothesized, males altered their behavior by increasing courtship and monitoring their nest when a rival was visible. This increase in courtship is in contrast to most studies on courtship in the presence of a rival that find a reduction in courtship behavior. Males spent more time opercular gill flaring when no barriers were present, suggesting that males may be trying to court the female and communicate to the rival simultaneously. There was also a trend for aggression toward the female and the rival to decrease as screen length increased. Thus, males compensate for the presence of a rival by adjusting their courtship and aggressive behaviors, which could have important implications for courtship success.     

Evolutionary interplay between ecology,morphology and reproductive behavior in threespine stickleback,Gasterosteus aculeatus

Synopsis Throughout its range, freshwater populations in the Gasterosteus aculeatus species complex display remarkable differentiation of morphology and behavior, much of which reflects differences in ecological conditions among habitats. We first describe the ecological conditions that have led to morphological and behavioral divergence in two common lake types in British Columbia, Canada. Deep, oligotrophic lakes have favored the evolution of slender fish well adapted for feeding on plankton (limnetic, sensu McPhail 1984), whereas shallow, more eutrophic lakes with extensive littoral zones favor fish that are deeper-bodied and well adapted for feeding on benthic invertebrates. The latter forage in large groups that attack nests guarded by males and cannibalize the young within. Courtship in these lakes is relatively inconspicuous, a feature that apparently enhances nest survivorship. In limnetic populations, this form of cannibalism is usually absent and courtship is conspicuous. Because benthic populations tend to have larger bodies and hence, larger gapes than do limnetic fish we suggest that cannibalism may be facilitated by large body size or a correlated trait. We test this by comparing the morphology of populations exhibiting both group cannibalism and a second kind of cannibalism in which solitary females court males, gain access to nests as a consequence, and then cannibalize eggs without spawning. Our results suggest that differences in body size cannot explain variation among populations in cannibalistic tendencies but that body size may affect the effectiveness of cannibalism by females within populations.     

Genetics of incipient speciation in Drosophila mojavensis. I. Male courtship song, mating success, and genotype x environment interactions

Few studies have examined genotype by environment (GxE) effects on premating reproductive isolation and associated behaviors, even though such effects may be common when speciation is driven by adaptation to different environments. In this study, mating success and courtship song differences among diverging populations of Drosophila mojavensis were investigated in a two-environment quantitative trait locus (QTL) analysis. Baja California and mainland Mexico populations of D. mojavensis feed and breed on different host cacti, so these host plants were used to culture F2 males to examine host-specific QTL effects and GxE interactions influencing mating success and courtship songs. Linear selection gradient analysis showed that mainland females mated with males that produced songs with significantly shorter L(long)-IPIs, burst durations, and interburst intervals. Twenty-one microsatellite loci distributed across all five major chromosomes were used to localize effects of mating success, time to copulation, and courtship song components. Male courtship success was influenced by a single detected QTL, the main effect of cactus, and four GxE interactions, whereas time to copulation was influenced by three different QTLs on the fourth chromosome. Multiple-locus restricted maximum likelihood (REML) analysis of courtship song revealed consistent effects linked with the same fourth chromosome markers that influenced time to copulation, a number of GxE interactions, and few possible cases of epistasis. GxE interactions for mate choice and song can maintain genetic variation in populations, but alter outcomes of sexual selection and isolation, so signal evolution and reproductive isolation may be slowed in diverging populations. Understanding the genetics of incipient speciation in D. mojavensis clearly depends on cactus-specific expression of traits associated with courtship behavior and sexual isolation.     

Peculiarities of the courtship song in the <Emphasis Type="Italic">Drosophila melanogaster</Emphasis> populations adapted to gradient of microecological conditions

In theory of evolution, two chief scenarios of development of sexual isolation—allopatric and sympatric, which act respectively under conditions of geographic separation or without it, are considered. Differences in the courtship behavior and in the used signals can lead to reproduction isolation and prevent gene exchange between sympatric populations or species, in which postmating barriers are absent. The previous studies of natural Drosophila populations inhabiting the opposite, ecologically contrast slopes of evolutional canyon (vicinities of the brook Oren in the mountain ridge Karmel, Israel) revealed statistically significant differences between them by the complex of adaptive and behavioral parameters including courtship behavior and choice of partner for mating. Astonishingly, differentiation of two populations has appeared in spite of a very small distance between two slopes. Here we report the statistically significant differences between males from the opposite slopes in characteristics of the courtship song that is one of signals serving for recognition by female of sexual partner of her species. We suggest that these differences can underlie the earlier revealed female discriminational behavior and can reflect different adaptive strategies in the populations inhabiting opposite canyon slopes.     

The effects of reproduction on courtship, fertility and longevity within and between alternative male mating tactics of the horned beetle, Onthophagus binodis

Life history theory provides a powerful tool to study an organism's biology within an evolutionary framework. The notion that males face a longevity cost of competing for and displaying to females lies at the core of sexual selection theory. Likewise, recent game theory models of the evolution of ejaculation strategies assume that males face a trade-off between expenditure on the ejaculate and expenditure on gaining additional matings. Males of the dung beetle Onthophagus binodis adopt alternative reproductive tactics in which major males fight for and help provision females, and minor males sneak copulations with females that are guarded by major males. Minor males are always subject to sperm competition, and consistent with theoretical expectation, minor males have a greater expenditure on their ejaculate than major males. We used this model system to seek evidence that mating comes at a cost for future fertility and/or male expenditure on courtship and attractiveness, and to establish whether these traits vary between alternative mating tactics. We monitored the lifespan of males exposed to females and nonmating populations, and sampled males throughout their lives to assess their fertility and courtship behaviour. We found a significant longevity cost of reproduction, but no fertility cost. On average, males from mating populations had a lower courtship rate than those from nonmating populations. This small effect, although statistically nonsignificant, was associated with significant increases in the time males required to achieve mating. Minor males had lower courtship rates than major males, and took longer to achieve mating. Although we did not measure ejaculate expenditure in this study, the correlation between lower courtship rate and longer mating speed of minor males documented here with their greater expenditure on the ejaculate found in previous studies, is consistent with game theory models of ejaculate expenditure which assume that males trade expenditure on gaining matings for expenditure on gaining fertilizations.     

The effect of sex and shoal size on shoaling behaviour in Danio rerio

Male and female zebra fish Danio rerio were given choices of shoals that differed in sex and size. Male zebra fish preferred to associate with female shoals over male shoals, but had no preference when given a choice between a mixed‐sex shoal and either a male or female shoal. Female zebra fish showed no significant preference when given a choice between male and females shoals, nor between mixed‐sex shoals and either male or female shoals. When given choices between shoals of differing size, females preferred to associate with the larger shoal, whether or not they were composed of males or females. Males, however, had no preference for larger shoals over smaller shoals, whether or not they were composed of males or females. These results showed that male zebra fish were capable of distinguishing between males and females solely on the basis of visual cues. Furthermore, these results demonstrated a significant difference between the shoaling choices of male and female zebra fish, which may indicate a difference in the function of shoaling for the two sexes.