Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish

Rapid speciation in Lake Victoria cichlid fish of the genus Pundamilia may be facilitated by sexual selection: female mate choice exerts sexual selection on male nuptial coloration within species and maintains reproductive isolation between species. However, declining water transparency coincides with increasingly dull coloration and increasing hybridization. In the present study, we investigated the mechanism underlying this pattern in Pundamilia nyererei, a species that interbreeds with a sister species in turbid but not in clear water. We compared measures of intraspecific sexual selection between two populations from locations that differ in water transparency. First, in laboratory mate‐choice experiments, conducted in clear water and under broad‐spectrum illumination, we found that females originating from turbid water have significantly weaker preferences for male coloration than females originating from clear water. Second, both the hue and body coverage of male coloration differ between populations, which is consistent with adaptation to different photic habitats. These findings suggest that the observed relationship between male coloration and water transparency is not mediated by environmental variation alone. Rather, female mating preferences are indicated to have changed in response to this variation, constituting the first evidence for intraspecific preference‐trait co‐evolution in cichlid fish. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 398–406.     

Premating Avoidance of Inbreeding Absent in Female Guppies (Poecilia reticulata)

The recognition and avoidance of kin during mating can be an important means of reducing the potential for inbreeding depression in offspring. We report here that premating mechanisms to avoid inbreeding, either innate or learnt through juvenile experience, are at best weak in female guppies (Poecilia reticulata). Guppies are small, ovoviviparous, neo‐tropical freshwater fish, with a polygamous mating system where males actively court females and females are selective of their mates. In a series of mate‐choice experiments, naïve, virgin females of the Quare River population in Trinidad were given a choice between a brother and a non‐sib male from the same population. Initially, females were only provided olfactory cues upon which to base their choice and then subsequently both olfactory and visual cues. Despite the females displaying mate choice, we found no evidence of them discriminating between the male types in either experiment. There was thus no indication of inbreeding avoidance, suggesting that experiences after maturation or with mature males (e.g. rare male preference), dispersal and/or post‐mating mechanisms may be evolutionarily more important avoidance mechanisms.     

The Disruption Hypothesis Does Not Explain Mate‐Choice Copying in the Guppy (Poecilia reticulata)

In some species, female mate choice is non‐independent as, under certain circumstances, females may copy the mate choice of other nearby females. One standard experimental protocol used to test for mate‐choice copying is the mate‐choice ‘reversal’ protocol. In this protocol, a focal female is allowed to choose between two males as potential mates and then is presented with an opportunity to see another female (i.e. the model female) choose the male that she did not initially choose. The focal is subsequently allowed to again choose between the same set of males. An observed reversal of her initial choice in this second preference test has been previously interpreted as evidence for mate‐choice copying. Alternatively, it has recently been proposed that environmental events, such as seeing the mate choice of nearby females that occur within the visual field of a female actively engaged in mate assessment, may ‘disrupt’ her decision‐making behavior and consequently alter the consistency of her mating preference, and may thus cause mate‐choice reversals. The disruption hypothesis predicts that if a model female is placed near the male that the focal female initially chose, the latter's mate preference would be disrupted and she would subsequently and consistently prefer the male that she initially rejected. Here we examined whether the disruption hypothesis explains mate‐choice copying in the guppy (Poecilia reticulata). Our results do not support this hypothesis, but rather provide further support for mate‐choice copying in the guppy.     

Mate Choice Copying in Female Humpback Limia (Limia nigrofasciata, Family Poeciliidae)

Mate choice copying is a mechanism of non‐independent mate choice that has important implications for models of evolution and sexual selection. In this study, we examined copying behavior in female humpback limia (Limia nigrofasciata). In three experiments, we allowed a focal female to choose between two males on opposite sides of an aquarium, then repeated the choice trial with the following modifications: (i) with no model female, (ii) with a model female added adjacent to the initially non‐preferred male, or (iii) with the model female adjacent to the initially preferred male. In the absence of other females, focal females displayed consistent mate preferences, measured as a significantly higher amount of time spent near the preferred male in both parts of the trial. When a model female was added adjacent to the initially non‐preferred male, focal females spent significantly more time near that male than they had in the first part of the trial, and significantly less time near the male they had initially preferred. When we placed the model female next to an initially preferred male as a control, the time spent by the focal female with the initially preferred or initially non‐preferred male did not change significantly. We conclude that female mate choice copying may be important in humpback limia, causing focal females to spend more time in preference zones of males they had not at first preferred.     

Innate and Learned Colour Preference in the Zebrafish, Danio rerio

Receiver biases towards specific sensory signals have been demonstrated in insects, birds and fish, both in the context of foraging and mate choice. In some cases, signals important in sexual selection appear to have evolved by exploiting a pre-existing bias in the sensory system. For instance, female preferences for male nuptial colouration may have arisen from selection on foraging practices. Using the zebrafish ( Danio rerio ), a species in which red is not a factor in mate choice, we tested for a foraging bias towards the colour red. We further investigated the plasticity of foraging biases by raising groups of fish on diets consisting solely of red, blue, green or white food. When we subsequently tested their colour preferences in a foraging context, each group responded most strongly to red, irrespective of the colour of food with which they had been conditioned. We also detected a significant effect of conditioning on colour preferences; fish responded more strongly to the colour that matched diet colour than to other colours. The observed receiver bias towards red may have evolved as an adaptive preference for carotenoid compounds in their diet. While the bias to red appears to be innate, our results indicate that learning is also important in shaping foraging biases.     

Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback

Mating isolation is a frequent contributor to ecological speciation – but how consistently does it evolve as a result of divergent selection? We tested for genetically based mating isolation between lake and stream threespine stickleback (Gasterosteus aculeatus L.) from the Misty watershed, Vancouver Island, British Columbia. We combined several design elements that are uncommon in the studies of stickleback mate choice: (i) we used second‐generation laboratory‐reared fish (to reduce environmental and maternal effects), (ii) we allowed for male–male competitive interactions (instead of the typical no‐choice trials) and (iii) we included hybrids along with pure types. Males of different types (Lake, Inlet, hybrid) were paired in aquaria, allowed to build nests and then exposed sequentially to females of all three types. We found that Lake and Inlet males differed in behaviours thought to influence stickleback mate choice (inter‐ and intra‐sexual aggression, display and nest activities), whereas hybrids were either intermediate or apparently ‘inferior’ in these behaviours. Despite these differences, Lake and Inlet fish did not mate assortatively and hybrid males did not have a mating disadvantage. Our study reinforces the noninevitability of mating isolation evolving in response to ecological differences and highlights the need to further investigate the factors promoting and constraining progress towards ecological speciation.     

Does Female Personality Determine Mate Choice Through Sexual Cannibalism?

Animal personalities (e.g. consistent across‐context behavioural differences between individuals) can lead to differences in mate choice. However, evidence for this link remains limited. Pre‐mating sexual cannibalism can be a behavioural syndrome (i.e. a suboptimal personality) in which adaptive female aggression towards heterospecific prey spills over on non‐adaptive aggression towards courting males, independently of the female mating or feeding status (i.e. the ‘aggressive spillover hypothesis’, ASH). On the other hand, sexual cannibalism can also be a form of mate choice by which females selectively kill or mate with males depending on the male phenotype. We introduce the hypothesis that the most aggressive females in the population will not only attack males more frequently, but will be less likely to impose sexual selection on males through sexual cannibalism. Assuming that in a field common garden experiment in which females were fed ad libitum the rate of weight gain by a female may reflect her voracity or aggressiveness, we show that in the cannibalistic burrowing wolf spider Lycosa hispanica (formerly L. tarantula), voracity towards heterospecific prey predicts a female's tendency towards sexual cannibalism. Unmated females with higher weight gains were more cannibalistic and attacked males regardless of the male phenotype. On the other hand, females that were less voracious tended to be less cannibalistic, and when they did kill a male, they were selective, killing males in poorer condition and mating with those in better condition. Our results demonstrate that females with different phenotypes (growth rates) differently imposed selection on male condition, tentatively supporting the hypothesis that female aggression levels can spill over on sexual selection through sexual cannibalism.     

Male mate choice in the Andrew’s toad <Emphasis Type="Italic">Bufo andrewsi</Emphasis>: a preference for larger females

In amphibians, theory predicts that male mate choice with respect to female body size can be expected to occur when female fecundity is related to body size and when the time and energy invested into one mating are relatively large. Based on experimental observations, we tested whether male mate choice occurs in a population of the Andrew’s toad (Bufo andrewsi), a species in which both assumptions are likely to be met. When a male B. andrewsi was placed with a gravid female and a non-gravid similar-sized female, the male did not discriminate between them. When two gravid females with distinct size differences were provided to a male, the male preferred the larger one. In an experiment in which two different-sized gravid females were put in two separate transparent cylinders to exclude potential chemical cues, males spent more time in proximity to the larger gravid females and jumped more frequently towards the larger gravid females than the smaller ones. These findings suggest that male B. andrewsi recognizes female body size, exhibits mate choice, and prefers to mate with larger females that provide greater reproductive potential.     

MATE CHOICE FOR NONADDITIVE GENETIC BENEFITS CORRELATE WITH MHC DISSIMILARITY IN THE ROSE BITTERLING (RHODEUS OCELLATUS)

Good genes models of mate choice predict additive genetic benefits of choice whereas the compatibility hypothesis predicts nonadditive fitness benefits. Here the Chinese rose bitterling, Rhodeus ocellatus, a freshwater fish with a resource‐based mating system, was used to separate additive and nonadditive genetic benefits of female mate choice. A sequential blocked mating design was used to test female mate preferences, and a cross‐classified breeding design coupled with in vitro fertilizations for fitness benefits of mate choice. In addition, the offspring produced by the pairing of preferred and nonpreferred males were reared to maturity and their fitness traits were compared. Finally, the MHC DAB1 gene was typed and male MHC genotypes were correlated with female mate choice. Females showed significant mate preferences but preferences were not congruent among females. There was a significant interaction of male and female genotype on offspring survival, rate of development, growth rate, and body size. No significant male additive effects on offspring fitness were observed. Female mate preferences corresponded with male genetic compatibility, which correlated with MHC dissimilarity. It is proposed that in the rose bitterling genetic compatibility is the mechanism by which females obtain a fitness benefit through mate choice and that male MHC dissimilarity, likely mediated by odor cues, indicates genetic compatibility.     

Female Size Influences Mate Preferences of Male Guppies

Guppies (Poecilia reticulata) have a promiscuous mating system in which female choice for brightly coloured males plays an important role. Consequently, much research on guppies has examined how mate choice by females has lead to the evolution of male colour patterns. Much less attention has been devoted to mate choice by males in this species. In this study, we show that male guppies are choosy when selecting a female to associate with, significantly preferring the larger female when presented with two females that differed by ≥2 mm in standard length (SL). The strength of their preference for each female increased with absolute female size. The relative sizes of the females, however, also influenced male mating preferences: males showed stronger preferences for the larger female as the difference in SL between the two females increased. Such a preference for larger females is not unexpected as fecundity generally increases with body size in female fish. Thus, males choosing to mate with the larger female should have higher reproductive success. An apparent, but non‐significant anomaly, whereby males appear to prefer the smaller of the two females when the difference between female SL was <4 mm, deserves further investigation.     

Male House Finches with Elaborate Songs have Higher Reproductive Performance

The elaborate songs of male animals are thought to function in either territory defense (male–male communication) or mate attraction (male–female communication). In non‐territorial animals, male vocalizations are expected to function primarily in mate attraction, yet the reproductive consequences of male vocalizations in non‐territorial animals are poorly described. Here we explore the relationship between male song and male reproductive performance in a free‐living population of house finches, Carpodacus mexicanus, a non‐migratory, non‐territorial songbird. Based on recordings of 20 males, we analyzed three song features (song length, number of unique syllables per song, and song rate) and compared male song with two measures of within‐pair reproductive performance (nest initiation date and clutch size) and one measure of extra‐pair reproductive performance (whether males sired extra‐pair young). We demonstrate a positive association between male song and within‐pair reproductive performance; males that sang long songs initiated their first clutch significantly earlier and males that sang songs at a faster rate had larger clutches. Despite the fact that only one of our recorded males sired extra‐pair young in the nest of another male, this male's songs were the most elaborate for two of three song features measured, anecdotally suggesting that male song may play a role in both within‐pair and extra‐pair partner choice. These results suggest that male song is a sexually selected trait in non‐territorial house finches.     

Female mate choice in relation to heterozygosity in Tribolium castaneum

Abstract Female mate choice, both before and after copulation, is pervasive among insect species. It is often hypothesized that females would preferentially mate with males that are genetically dissimilar to promote the genetic variability of the offspring. We used various strains of red flour beetle, Tribolium castaneum, and tested the effect of male and female genetic backgrounds on precopulatory and post‐copulatory female mate choice. Simultaneous mate choice experiments using previously well established pheromone assays did not detect female preference for males of different strains. Post‐copulatory female mate choice was examined through paternity analysis. Two parameters were used to measure post‐copulatory female mate choice, including male defence capacity (P₁, proportion of offspring sired by the first male when a female mated with two males consecutively) and offence capacity (P₂, proportion of offspring sired by the second of two males to mate with a female). When female and male beetle strains were same, defence capacity was significantly higher than when female and male strains were different. However, such a pattern was not observed for offence capacity. The results suggest that female precopulatory mate choice is not affected by genetic background, but the outcome of post‐copulatory processes depends on the genetic background of male and female beetles.     

Tail Length and Mutual Mate Choice in Bearded Tits (Panurus biarmicus)

Direct sexual selection via mutual mate choice can result in both sexes showing conspicuous traits. We experimentally tested whether this hypothesis can explain tail length in the bearded tit (Panurus biarmicus). In this species, both sexes have a long, graduated tail. Males have, however, a longer tail than females, suggesting perhaps that females are choosier than males in selecting mates. We used two choice set‐ups for each sex: shortened vs. control tail individuals and elongated vs. control tail individuals. We found that direct sexual selection seems to operate differently in the two sexes. In both set‐ups, females spent more time with the male with the longest tail, and they also showed sexual display behaviour only towards these males. Males spent more time with control than with short‐tailed females, but they did not discriminate between control and long‐tailed females. Moreover, males displayed preference towards both short‐ and long‐tailed females. Thus, females preferred long‐tailed males, whereas males did not always prefer long‐tailed females. Our study suggests that mutual mate choice has played a role in the evolution of long tails in bearded tits. It also suggests that the sexual dimorphism in tail length has evolved because mate choice exerts a stronger sexual selection pressure on males than on females.     

How Do Females’ Genetic Characteristics Influence Male Mate Preference in the Terrestrial Isopod Armadillidium vulgare?

Genetic diversity is a key factor that can influence mate choice in many species. We experimentally determined the influence of this factor on mate preference in the crustacean terrestrial isopod Armadillidium vulgare. This biological model is gregarious which could increase the risk of inbreeding by mating with closely related partners. Mechanisms of inbreeding avoidance during mate choice can thus be expected. Moreover, previous studies predict that males would be the choosy sex. We performed Y‐choice tests giving males the choice between two females presenting different levels of heterozygosity and genetic similarity to the male. Our results show potential inbreeding avoidance according to the genetic characteristics of females presented to males. The higher the variation in genetic similarity to the male between females is, the higher the preference of the male towards the most dissimilar female is. Hence, male preferences may only be detectable when the difference between females’ genetic characteristics is large enough. If heterozygosity is associated with fitness in A. vulgare (as in many organisms), the patterns of mate preference we observe may be adaptive.     

Sexual Selection on male cuticular hydrocarbons via male–male competition and female choice

Traditional views of sexual selection assumed that male–male competition and female mate choice work in harmony, selecting upon the same traits in the same direction. However, we now know that this is not always the case and that these two mechanisms often impose conflicting selection on male sexual traits. Cuticular hydrocarbons (CHCs) have been shown to be linked to both social dominance and male attractiveness in several insect species. However, although several studies have estimated the strength and form of sexual selection imposed on male CHCs by female mate choice, none have established whether these chemical traits are also subject to sexual selection via male–male competition. Using a multivariate selection analysis, we estimate and compare sexual selection exerted by male–male competition and female mate choice on male CHC composition in the broad‐horned flour beetle Gnatocerus cornutus. We show that male–male competition exerts strong linear selection on both overall CHC abundance and body size in males, while female mate choice exerts a mixture of linear and nonlinear selection, targeting not just the overall amount of CHCs expressed but the relative abundance of specific hydrocarbons as well. We discuss the potential implications of this antagonistic selection with regard to male reproductive success.     

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.     

Non‐Visual Mate Choice Ability in a Cavefish (Poecilia mexicana) is not Mechanosensory

One of the most important decisions any female has to make is selecting a mate. In many animals, this involves a strong visual component, but in cave‐dwelling fishes, mate preferences have to be exercised in darkness. In a cave‐dwelling Poeciliid fish, the cave molly (Poecilia mexicana), visual mate choice is still possible because they have functional, albeit reduced eyes. In a previous laboratory study, it was documented that females prefer larger males in light and in darkness. In the present study, we investigated the role of the mechanosensory lateral line in this mate preference. We temporarily knocked out the lateral line using antibiotics. We found that even in the functional absence of the lateral line, females showed a clear preference for larger males, indicating that the lateral line is not crucial for mate choice. This points toward a strong role of chemical communication in cave molly mate choice.     

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

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

Strategic mate‐guarding behaviour in ladybirds

Mate‐guarding behaviour is regarded as a means of increasing paternity share by reducing sperm competition. It is known to be a plastic response which varies with operational sex ratios and competitor presence in the vicinity. In a recent study, prolonged mating duration in Menochilus sexmaculatus (Fabricius) (Coleoptera: Coccinellidae) has been found to incorporate mate‐guarding behaviour. The present investigation was conducted to assess its plasticity in the presence of competitors. The physical and chemical presence of competitors of both sexes at varying densities was provided to a pair of ladybirds, and their time to commence mating, latent period and mate‐guarding duration was observed. These were compared to a control treatment where other partners were absent. All treatments were conducted with sibling as well as non‐sibling competitors. It was our hypothesis that mate guarding would be increased in the presence of male competitors and would be reduced by female presence. The results revealed that while mate‐guarding duration was increased by the chemical presence of males it was decreased by their physical presence. The latter result was attributed to interference by other males who dislodge the mating male in order to access the female. Female chemical presence had no effect on mate guarding, while physical presence increased the duration of mate guarding. The reasons for the latter behaviour require further investigation. Responses were not significantly affected by the relationship between the focal pair and the competitor. The authenticity of the mate guarding in this ladybird is strongly affirmed by our results.     

Experimental evidence for a hierarchy of mate- and host-induced cues in a fish ectoparasite, Argulus coregoni (Crustacea: Branchiura)

Argulus coregoni is an ectoparasite primarily infesting freshwater salmonids. Sexually reproducing parasites such as A. coregoni are confronted with a dilemma between finding a mate and the costs involved in doing so; if mating partners are unavailable on a host, by leaving to search for a mate on a new host, the parasite is exposed to risks such as predation and energy loss. The utilization of chemical cues could enhance the probability of finding a host and/or a suitable mating partner and thus decrease the level of costs associated with detachment from the host. In this study we constructed a Y-maze arena to determine if adult A. coregoni respond to mate- and host-related chemical cues. We also tested the directional response towards light, since it has been suggested that photic cues are the most important cues for juvenile A. coregoni locating a host. Our results showed that both sexes were attracted to light and fish odour. Free-swimming A. coregoni males responded to chemical cues produced by adult females but not vice versa. The hierarchy of these stimuli was analyzed by pitting the cues against one another in the Y-maze, showing that light was the most salient stimulus for both male and female parasites. Moreover, male parasites were more strongly attracted towards light and fish odour than female odour. In another experiment in a semi-natural environment, we examined whether the ability of A. coregoni males to detect female odour influences their host choice. Free-swimming males did not preferentially infest fish infected with female parasites over parasite-free fish. We suggest that a hierarchy of stimulus responses exists, whereby free-swimming parasites first respond to host-related signals and most dominantly to visual cues. However, cues connected to mate finding may become a priority for late adult stages and/or once the parasite has attached to the host.