The impact of social context on male mate preference in a unisexual--bisexual mating complex

Male sailfin mollies Poecilia latipinna were tested in five different treatments that varied in the relative frequency of heterospecific gynogens (Amazon molly Poecilia formosa) to conspecific females to determine whether social interactions among males within a population causes some males to mate with heterospecific females. Male P. latipinna inseminated a significantly higher proportion of conspecific females and fertilized a significantly higher number of conspecific eggs regardless of the treatment. Nonetheless, preference for conspecific females was not exclusive as a range of 20 to 50% of heterospecific females were fertilized. Social interactions among males may best explain the results and may therefore play an important role in the maintenance of unisexual--bisexual mating complexes.     

Female sperm limitation in natural populations of a sexual/asexual mating complex (Poecilia latipinna, Poecilia formosa)

In sperm-dependent sexual/asexual mating systems, male mate choice is critical for understanding the mechanisms behind apparent stability observed in natural populations. The gynogenetic Amazon molly (Poecilia formosa) requires sperm from sexual males (e.g. Poecilia latipinna) to trigger embryogenesis, but inheritance is strictly maternal. Consequently, males should try to avoid or reduce the cost of mating with asexuals. We investigated male mate choice by documenting the presence of sperm in natural populations and found that a higher proportion of sexual females had sperm than asexuals. In addition, among those females that had sperm, sexuals had more sperm than asexuals. Our results hint at a role for male mate choice as a stabilizing factor in such systems.     

Male mate choice and sperm allocation in a sexual/asexual mating complex of Poecilia (Poeciliidae, Teleostei)

Male mate choice is critical for understanding the evolution and maintenance of sexual/asexual mating complexes involving sperm-dependent, gynogenetic species. Amazon mollies (Poecilia formosa) require sperm to trigger embryogenesis, but the males (e.g. Poecilia mexicana) do not contribute genes. Males benefit from mating with Amazon mollies, because such matings make males more attractive to conspecific females, but they might control the cost of such matings by providing less sperm to Amazon mollies. We examined this at the behavioural and sperm levels. P. mexicana males preferred to mate with, and transferred more sperm to conspecific females. However, if males mated with P. formosa, sperm was readily transferred. This underscores the importance of male choice in this system.     

Geographical variation in reproductive character displacement in mate choice by male sailfin mollies

Female Amazon mollies, Poecilia formosa, are a unisexual species that reproduce by gynogenesis. They must coexist and mate with males of other species (usually the mollies Poecilia latipinna or Poecilia mexicana) to induce embryogenesis, but inheritance is strictly maternal. We examined the mating preference of the male sailfin molly, P. latipinna, for female sailfin mollies versus Amazon mollies, P. formosa. We compared the mating preferences of sympatric and allopatric populations collected throughout the Gulf Coast of North America. Male P. latipinna from six populations sympatric with Amazon mollies showed a significantly greater strength of preference for conspecific sailfin females than males from five populations that were allopatric with Amazon mollies. These results provide strong evidence for reproductive character displacement of male mate choice in sympatry. Furthermore, the large geographical range of populations that we tested revealed variation among populations within sympatry and allopatry, indicating that it is important to evaluate a large number of populations when examining reproductive character displacement.     

Parasites in sexual and asexual mollies (Poecilia, Poeciliidae, Teleostei): a case for the Red Queen?

The maintenance of sexual reproduction in the face of its supposed costs is a major paradox in evolutionary biology. The Red Queen hypothesis, which states that sex is an adaptation to fast-evolving parasites, is currently one of the most recognized explanations for the ubiquity of sex and predicts that asexual lineages should suffer from a higher parasite load if they coexist with closely related sexuals. We tested this prediction using four populations of the sexual fish species Poecilia latipinna and its asexual relative Poecilia formosa. Contrary to expectation, no differences in parasite load could be detected between the two species.     

Sexual harassment in live-bearing fishes (Poeciliidae): comparing courting and noncourting species

Sexual harassment by males has been reported from several live-bearingfishes (Poeciliidae) and has been shown to inflict costs onfemales. For example, poeciliid females have reduced feedingopportunities when accompanied by a male because females dedicateattention to avoiding male copulation attempts. Poeciliid speciesdiffer considerably in male mating behavior, such as the presenceor absence of courtship. Courting males display in front ofthe females, but males attempting to sneak-copulate approachfemales from behind, that is, in the blind portion of theirvisual field, and force copulations, which can be viewed asa male persistence trait. We predicted that poeciliid femalesneed to be more vigilant in the presence of noncourting males,and costs of harassment by noncourting males might be stronger.In a comparative approach we examined the costs of male sexualharassment for females as reduced feeding time in 9 speciesof live-bearing fishes, including courting (Poecilia latipinna,Poecilia reticulata, Xiphophorus cortezi, Xiphophorus variatus)and noncourting species (Poecilia mexicana [surface- and cave-dwellingform], Poecilia orri, Gambusia affinis, Gambusia geiseri, Heterandriaformosa). In all species examined except for the cave form ofP. mexicana, focal females spent significantly less time feedingin the presence of a male than when together with another female.The time females spent feeding was found to significantly declinewith increasing male mating activity (sum of all sexual behaviors),but there was no support for the idea that females would spendmore time feeding in the presence of courting males comparedwith noncourting ones.     

How to go extinct by mating too much: population consequences of male mate choice and efficiency in a sexual–asexual species complex

Selection acting on individuals is not predicted to maximize population persistence, yet examples that explicitly quantify conflicts between individual and population level benefits are scarce. One such conflict occurs over sexual reproduction because of the cost of sex: sexual populations that suffer the cost of producing males have only half the growth rate compared to asexuals. Male behaviour can additionally impact population dynamics in a variety of ways, and here we study an example where the impact is unusually clear: the riddle of persistence of sperm‐dependent sexual–asexual species complexes. Here, a sexually reproducing host species coexists with an ameiotically reproducing all‐female sperm parasite. Sexual–asexual coexistence should not be stable because the proportion of asexually reproducing females will rapidly increase and the relative abundance of the sexually reproducing host species will decline. A severe shortage of males will lead to sperm limitation for sexual and asexual females and the system collapses. Male mate choice could reduce the reproductive potential of the asexual species and thus potentially prevent the collapse. In the gynogenetic (sperm‐dependent parthenogenetic) Amazon molly Poecilia formosa and its host (P. latipinna or P. mexicana), males discriminate against asexual females to some extent. Using a population‐dynamical model, we examine the population dynamics of this species complex with varying strengths of male discrimination ability and efficiency with which they locate females and produce sperm. The sexual species would benefit from stronger discrimination, thus preventing being displaced by the asexual females. However, males would be required to evolve preferences that are probably too strong to be purely based upon selection acting on individuals. We conclude that male behaviour does not fully prevent but delays extinction, yet this is highly relevant because low local extinction rates strongly promote coexistence as a metapopulation.     

PEERING THROUGH THE LOOKING GLASS AT A SEXUAL PARASITE: ARE AMAZON MOLLIES RED QUEENS?

Abstract.— The gynogenetic Amazon molly ( Poecilia formosa ) is a clonal, all-female lineage of livebearing fish that faces an unusual obstacle to evolutionary persistence. Sperm from heterospecific males (either sailfin, P. latipinna , or Atlantic, P. mexicana , mollies) is necessary to trigger embryogenesis. However, none of the male's genes are incorporated into the genome of the gynogenetic offspring. Some investigators have proposed that the evolution of male mate discrimination is a result of this cost, leading to a coevolutionary arms race between male avoidance of P. formosa and P. formosa attractiveness. Given that P. formosa successfully reproduces and has not yet gone extinct, it is clear there are mechanisms by which they attract the sexual attention of males. Although a Red Queen coevolutionary process in typical host/parasite systems has been shown to favor the persistence of sexual species, in this system an arms race has been invoked to explain the reverse. Here I present behavioral data supporting a more parsimonious scenario: that mechanisms of attraction in P. formosa are simply a consequence of its hybrid origin. Poecilia latipinna and P. mexicana males do not discriminate between gynogenetic P. formosa females and first generation sexual hybrid females, and females do not differ in agonistic behaviors associated with competition for mates. Both results contradict predictions from the Red Queen hypothesis. Therefore, coevolution is not necessary to explain the apparent evolutionary persistence of P. formosa.     

Spectral sensitivity of mollies: comparing surface- and cave-dwelling Atlantic mollies, Poecilia mexicana

The visual pigments of cones and rods in three species of mollies, Poecilia mexicana , Poecilia latipinna and their asexual hybrid Poecilia formosa , were examined using microspectrophotometry. In P. mexicana , populations from extreme photic habitats were used: one population originated from a clear water habitat, one from a milky water habitat and another from a completely dark cave. Ultraviolet-sensitive cones were found in all species. Differences in the λ_max values of the visual pigments were small between species and among the three P. mexicana populations, but dark-reared cave fishes showed appreciably higher variance. The hybrid species P. formosa showed a highly variable long wavelength cone absorbance, ranging from 528·9 to 598·5 nm, suggesting multiple opsin expression or chromophore mixing.     

Male mate choice in the gynogenetic–sexual complex of crucian carp,<Emphasis Type="Italic"> Carassius auratus</Emphasis>

The asexual all-female Japanese crucian carp, Carassius auratus langsdorfii (Teleostei: Cypriniformes), reproduces gynogenetically, relying on the sperm of males of the sexual "host," C. auratus subspp. Theoretically, frequency-dependent mating preference of males to conspecific females can lead to the coexistence of asexual and sexual fish, if all else is equal. Our specific questions are whether males prefer conspecific females over asexual females and whether individuals show dominance hierarchies that potentially cause frequency-dependent mating preference. In an individual choice experiment, a tank was partitioned into three compartments with the middle one for a single male and the two outer ones for a sexual and an asexual female. The males of C. auratus bürgeri demonstrated a significant preference for ovulated conspecific females over ovulated asexual females. In contrast, in a group mating experiment, a single experimental tank included two males, a sexual female, and an asexual female together, and males chased and mated with both asexual and sexual females equally. Male mate preference was weak in group mating, which is typical in natural populations. Males and females of crucian carp showed no apparent agonistic behavior to each other in the group mating experiment. This is different from other gynogenetic complexes with the dominance hierarchy of males showing strong frequency-dependent mating preference (e.g., Poeciliopsis). We conclude that male mate preference is unlikely to be a strong frequency-dependent force maintaining the coexistence of asexual–sexual complexes of Japanese crucian carp. Received in revised form: 5 February 2001 Electronic Publication     

Dietary niche overlap in sympatric asexual and sexual livebearing fishes Poecilia spp

The present study investigated the spatiotemporal patterns in trophic resource use in a system of a gynogenetic poeciliid fish, the Amazon molly Poecilia formosa, and its sexual congeners the sailfin molly Poecilia latipinna and the Atlantic molly Poecilia mexicana using gut contents analysis. No statistically significant differences in trophic resource use were found between sexual and gynogenetic species, but gut contents varied significantly across sites and over time. In addition, variation in trophic morphology (i.e. gut length) was significant across sites but not species, and laboratory experiments indicated that gut length is phenotypically plastic. Overall, trophic differentiation between coexisting asexual and sexual Poecilia appears to be minimal, and it is unlikely that niche differentiation contributes to a stable coexistence of the two reproductive forms.     

Comparison of parasite communities in native and introduced populations of sexual and asexual mollies of the genus Poecilia

The parasite communities of two molly species, the sexual Poecilia latipinna and the clonal Poecilia formosa , were investigated in four populations using a novel method applicable under field conditions. In two native populations from south Texas and two introduced populations from central Texas, four species of microparasites and eight species of macroparasites were recorded. Virtually no differences in the parasite diversity and species composition could be detected between the populations. Mollies from south Texas had a higher individual parasitization index of macroparasites. There was a negative correlation between the relative number of oocytes in gravid females and their individual macroparasite load.     

A Sexual Preference in the Amazon Molly, Poecilia formosa

The Amazon molly, Poecilia formosa, is an all-female species that reproduces by gynogenesis, i.e., it relies on sperm of males of closely related species to trigger embryogenesis. Sperm is supplied by males of P. latipinna and P. mexicana. Amazon mollies live in sympatry with at least one of these species, a few populations live in sympatry with two sperm-donor species. As P. formosa is sperm dependent, it needs mechanisms for species and mate recognition. To investigate the effect of rearing conditions on sexual preferences of Amazon mollies, we raised Amazon mollies in sympatry with P. latipinna and P. mexicana males. We used simultaneous choice tests to determine the effect of age on female sexual preferences. Immature Amazon mollies do not exhibit a preference if given a choice between a P. latipinna and a P. mexicana male, whereas adult P. formosa do have a preference for the P. latipinna male. We used two different stimuli in this study, live males and videotapes of males.     

Monophyletic origin of multiple clonal lineages in an asexual fish (Poecilia formosa)

Despite the advantage of avoiding the costs of sexual reproduction, asexual vertebrates are very rare and often considered evolutionarily disadvantaged when compared to sexual species. Asexual species, however, may have advantages when colonizing (new) habitats or competing with sexual counterparts. They are also evolutionary older than expected, leaving the question whether asexual vertebrates are not only rare because of their 'inferior' mode of reproduction but also because of other reasons. A paradigmatic model system is the unisexual Amazon molly, Poecilia formosa, that arose by hybridization of the Atlantic molly, Poecilia mexicana, as the maternal ancestor, and the sailfin molly, Poecilia latipinna, as the paternal ancestor. Our extensive crossing experiments failed to resynthesize asexually reproducing (gynogenetic) hybrids confirming results of previous studies. However, by producing diploid eggs, female F(1) -hybrids showed apparent preadaptation to gynogenesis. In a range-wide analysis of mitochondrial sequences, we examined the origin of P. formosa. Our analyses point to very few or even a single origin(s) of its lineage, which is estimated to be approximately 120,000 years old. A monophyletic origin was supported from nuclear microsatellite data. Furthermore, a considerable degree of genetic variation, apparent by high levels of clonal microsatellite diversity, was found. Our molecular phylogenetic evidence and the failure to resynthesize the gynogenetic P. formosa together with the old age of the species indicate that some unisexual vertebrates might be rare not because they suffer the long-term consequences of clonal reproduction but because they are only very rarely formed as a result of complex genetic preconditions necessary to produce viable and fertile clonal genomes and phenotypes ('rare formation hypothesis').     

It's in the eye of the beholder: visual lateralisation in response to the social environment in poeciliids

The social environment offers fish complex information about the quality, performance, personality and other cues of potential mates and competitors simultaneously. It is likely, therefore, that the environmental information regarding the context of mate choice is perceived and processed differently in species and sexes in respect to lateralisation. The present study comparatively assessed visual lateralisation behaviour in response to different social or sexual stimuli in three closely related poeciliid species (P. latipinna, P. mexicana, P. formosa) in comparison to a more distantly related species (P. reticulata). Individuals were presented with four different social or sexual stimuli that were tested against a control stimulus; (a) a conspecific male, (b) a conspecific female, (c) a heterosexual conspecific pair, (d) three conspecific females (shoal). In order to approach a target stimulus, focal fish had to perform detours to the right or left of a vertically straight-shaped barrier. The three closely related poeciliid species, P. latipinna, P. mexicana, P. formosa, appeared to have a general tendency to turn right (i.e., left-eye preference), whereas the more distantly related P. reticulata males and females showed an overall bias to the left (i.e., right-eye preference) in response to various social–sexual incitements. Moreover, body size seemed to significantly influence especially the males’ detour behaviour, with smaller males acting in opposition to their larger conspecifics in response to certain social stimuli. In this case, smaller and larger Poecilia spp. males responded in the same way as smaller and larger males of the other three poeciliid species. Therefore, results possibly point to differences in the degree of general social behaviour between closely and more distantly related species and mating motivation amongst larger and smaller individuals when placed in a novel social environment. Hence, present results possibly suggest a sex-specific functional lateralisation for the analysis of visual information and seem to support the closer ancestral relationships between the Poecilia spp. tested in this study and the more distantly related guppies in terms of their left–right lateralisation. Generally, present results suggest that functional asymmetries in behaviour could be widespread among vertebrates, thus supporting the hypothesis of an early evolution of lateralisation in brain and behaviour.     

Lack of species discrimination based on chemical cues by male sailfin mollies, <Emphasis Type="Italic">Poecilia latipinna</Emphasis>

When making mating decisions, individuals may rely on multiple cues from either the same or multiple sensory modalities. Although the use of visual cues in sexual selection is well studied, fewer studies have examined the role of chemical cues in mate choice. In addition, few studies have examined how visual and/or chemical cues affect male mating decisions. Male mate choice is important in systems where males must avoid mating with heterospecific females, as is found in a mating complex of Poecilia. Male sailfin mollies, Poecilia latipinna, are sexually parasitized by gynogenetic Amazon mollies, P. formosa. Little is known about the mechanism by which male sailfin mollies base their mating decisions. Here we tested the hypothesis that male sailfin mollies from an allopatric and a sympatric population with Amazon mollies use multiple cues to distinguish between conspecific and heterospecific females. We found that male sailfin mollies recognized the chemical cues of conspecific females, but we found no support for the hypothesis that chemical cues are by themselves sufficient for species discrimination. Lack of discrimination based on chemical cues alone may be due to the close evolutionary history between P. latipinna and P. formosa. Males from populations sympatric with Amazon mollies did not differentially associate with females of either of the two species when given access to both visual and chemical cues of the females, yet males from the allopatric population did associate more with conspecific females than with heterospecific females in the presence of both chemical and visual cues. The lack of discrimination by males from the sympatric population between conspecific and heterospecific females based on both chemical and visual cues suggests that these males require more complex combinations of cues to distinguish species, possibly due to the close relatedness of these species.     

Hypoxia and interdemic variation in Poecilia latipinna

Variation in respiratory traits was quantified between two populations of the sailfin molly Poecilia latipinna (one from a periodically hypoxic salt marsh, Cedar Key, and one from a chronically normoxic river site, Santa Fe River). Two suites of characters were selected: traits that may show both short‐term acclimation response and interdemic variation in acclimation response (metabolic rate, critical oxygen tension and respiratory behaviour), and those that are not likely to respond to short‐term acclimation but may vary among populations (gill morphometric characters). Sailfin mollies from the salt marsh, acclimated to hypoxia (1 mg l⁻¹, c . 20 mmHg) for 6 weeks, spent less time conducting aquatic surface respiration and had lower gill ventilation rates than hypoxia‐acclimated conspecifics from the well‐oxygenated river site. Poecilia latipinna acclimated to hypoxia exhibited a lower critical oxygen tension ( P _c) than fish acclimated to normoxia; however, there was also a significant population effect. Poecilia latipinna from Cedar Key exhibited a lower P _c than fish from the Santa Fe River, regardless of acclimation. Cedar Key fish had a 14% higher mean gill surface area relative to fish from the Santa Fe River, a character that could account, at least in part, for their greater tolerance to hypoxia.     

Male Mate Choice in Mixed Bisexual/Unisexual Breeding Complexes of Poecilia (Teleostei: Poeciliidae)

The livebearing all-female fish Poecilia formosa reproduces by gynogenesis, a modified form of parthenogenesis. P. formosa forms at least two breeding complexes: in its northern range it exists sympatrically with Poecilia latipinna and in its southern range with Poecilia mexicana. Differences between these complexes and their possible origin are discussed. Embryogenesis is triggered by sperm of males of these closely related sympatric species. Because inheritance is strictly maternal, from the male point of view energy and time invested are totally lost. In this study we wanted to elucidate whether males are able to distinguish between conspecific and parasitic females. It could be shown that males are able to distinguish females optically, but that this ability was obscured as soon as chemical and/or tactile contact was possible. Furthermore, we found that females in an attractive phase of their sexual cycle are always preferred, regardless of species. This is possibly the mechanism by which parasitic females obtain the matings they need to reproduce.     

Males,but not females,contribute to sexual isolation between two sympatric species of <Emphasis Type="Italic">Gambusia</Emphasis>

Reproductive isolation restricts genetic exchange between species. Various pre- and post-mating barriers, such as behavior, physiology and gametic incompatibility, have been shown to evolve in sympatry. In certain scenarios, isolation can be asymmetrical, where species differentially prefer conspecifics. We examined sexual isolation via conspecific mate preference between Gambusia affinis and G. geiseri in both sexes. To investigate male contribution to sexual isolation, we compared the number of mating attempts (gonopodial thrusts) directed at either a conspecific or a heterospecific female, in both species. We also examined sperm priming and expenditure in males in the presence of conspecific or heterospecific females. We then measured female preference for either a conspecific or heterospecific male, in both species. We found that males of both species preferred to mate with conspecific females, but showed no difference in sperm production or expenditure between conspecific and heterospecific females. Females of both species did not prefer conspecific over heterospecific males. Our results suggest that sexual isolation might be mediated by male mate choice in this system and not female choice, suggesting that there is asymmetrical reproductive isolation between the sexes in G. affinis and G. geiseri, but symmetrical species isolation.     

Preference for conspecifics evolves earlier in males than females in a sexually dimorphic radiation of fishes

Speciation by sexual selection is generally modeled as the coevolution of female preferences and elaborate male ornaments leading to behavioral (sexual) reproductive isolation. One prediction of these models is that female preference for conspecific males should evolve earlier than male preference for conspecific females in sexually dimorphic species with male ornaments. We tested that prediction in darters, a diverse group of freshwater fishes with sexually dimorphic ornamentation. Focusing on the earliest stages of divergence, we tested preference for conspecific mates in males and females of seven closely related species pairs. Contrary to expectation, male preference for conspecific females was significantly greater than female preference for conspecific males. Males in four of the 14 species significantly preferred conspecific females; whereas, females in no species significantly preferred conspecific males. Relationships between the strength of preference for conspecifics and genetic distance revealed no difference in slope between males and females, but a significant difference in intercept, also suggesting that male preference evolves earlier than females’. Our results are consistent with other recent studies in darters and suggest that the coevolution of female preferences and male ornaments may not best explain the earliest stages of behavioral isolation in this lineage.