Behavioural and life‐history regulation in a unisexual/bisexual mating system: does male mate choice affect female reproductive life histories?

In theory, unisexual taxa have an advantage over ecologically similar bisexual species because unisexuals produce twice as many daughters and, thus, should quickly outcompete coexisting bisexuals in any given population. For sperm‐dependent unisexual (gynogenetic) species, stable coexistence with their bisexual sperm donors can be postulated if male mate choice puts unisexual females at a disadvantage through sperm limitation, thus halving their reproductive output compared to bisexuals (‘behavioural regulation hypothesis’). We tested for a potential life‐history signature of male mate choice in a system of coexisting bisexual sailfin mollies (Poecilia latipinna) and gynogenetic Amazon mollies (Poecilia formosa). Specifically, we gave P. latipinna males an opportunity to freely interact (and mate) with both types of females and, after 25 days, quantified the proportion of (1) females with sperm in their genital tract and (2) pregnant females. A higher proportion of P. latipinna females (53.7%) had sperm in their genital tract (compared to only 25.9% in P. formosa), corroborating a previous study on wild‐caught fish. This translated into a higher frequency (42.6%) of P. latipinna females being pregnant (compared to 29.6% in P. formosa); however, among pregnant females, no significant differences between species in reproductive life‐history traits (such as offspring number or size) were uncovered. Hence, although the findings of the present study confirm that male discrimination against unisexual females leads to reduced reproductive output in unisexuals, the observed magnitude of differences in targeted life histories between the two types of females is unlikely to be the sole factor regulating stable coexistence in this system. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 598–606.     

Do I Know You? Species Recognition Operates Within and Between the Sexes in a Unisexual–Bisexual Species Complex of Mollies

Male sailfin mollies (Poecilia latipinna) can be sexually parasitized by closely related, unisexual, gynogenetic Amazon mollies (Poecilia formosa). This study examined possible cues used by male P. latipinna to distinguish between conspecific females and sympatric, heterospecific P. formosa. Digital photos were used to create models to test male P. latipinna preference for model female P. latipinna and P. formosa with a full suite of traits and altered models of P. latipinna and P. formosa. Male P. latipinna significantly preferred models of either species over no stimulus, demonstrating that models elicit a male response. Males also significantly preferred female P. latipinna models over P. formosa models. We also examined species recognition by female sailfin mollies using the same models, and found that female sailfin mollies significantly preferred to associate with female P. latipinna over P. formosa. These results taken together suggest that the use of fish models yield results similar to those studies using live stimuli. Male preference was then tested for unaltered vs. altered models in the following combinations: (i) P. formosa vs. P. formosa with a female P. latipinna fin; (ii) P. formosa vs. P. formosa with a female P. latipinna lateral spot pattern; (iii) P. formosa vs. P. latipinna with a P. formosa fin and their spotless lateral pattern. Males did not significantly prefer models with any isolated traits over the unaltered P. formosa models. Thus, males may be using traits other than the ones isolated for species recognition or males may be using a suite of multiple traits to recognize conspecific females.     

Juvenile survival in a unisexual/sexual complex of mollies

Unisexual species like the gynogenetic Amazon molly, Poecilia formosa, enjoy a twofold advantage over sexual species, because they do not produce males. Therefore, unisexuals should be able to outcompete and consequently, replace sexual species. For sperm-dependent (gynogenetic) unisexuals this creates a paradox: they cannot replace their sexual hosts without eradicating themselves. Thus, mechanisms must be in place to stabilize such mating systems. We assessed juvenile survivorship between asexual P. formosa and sexual Poecilia latipinna as a possible factor allowing for persistence and coexistence between the two sympatric species. Offspring of gynogenetic Amazon mollies did not differ significantly in survivorship compared to their sexual host, the Sailfin molly, P. latipinna. The presence of an adult female significantly reduced survival in both species, suggesting that filial cannibalisms operates in this system, but does not appear to play a role in stabilizing mixed sexual/asexual populations. Clark Hubbs, who spent 59 years at the University of Texas and was widely regarded as one of the state’s foremost researchers in the field of ichthyology, the study of fish, passed away February 3rd of 2008 after a long battle with colorectal cancer. He was 86.     

Feeding rates in the sailfin molly Poecilia latipinna and its coexisting sexual parasite,the gynogenetic Amazon molly Poecilia formosa

Feeding rates of the gynogenetic Amazon molly Poecilia formosa and one of its sexual hosts, the sailfin molly Poecilia latipinna, were measured under winter and summer temperature conditions. Food consumption of the unisexual P. formosa in winter conditions was significantly higher than that of P. latipinna, and it is hypothesized that the resulting food stress might have an important influence on the population composition of these closely related fishes via higher winter mortality in P. formosa.     

Male mating behaviour of a molly, <Emphasis Type="Italic">Poecilia latipunctata</Emphasis>: a third host for the sperm-dependent Amazon molly, <Emphasis Type="Italic">Poecilia formosa</Emphasis>

The Tamesí molly, Poecilia latipunctata, has a very limited biogeographical range in northeast Mexico. This area is nested within the ranges of the Atlantic molly, Poecilia mexicana, and the unisexual Amazon molly, Poecilia formosa. Based on morphology, especially fin shape, the Tamesí molly has been considered to be a "short-fin" molly. We describe the courtship sequence of P. latipunctata. The courtship clearly places the species into the clade of "long-fin" mollies, a finding that corroborates earlier studies based on nuclear DNA and mitochondrial DNA. All three species live together in certain habitats. This renders P. latipunctata a potential host species for the sperm-dependent, unisexual Amazon molly. Using behavioural tests, we demonstrate that P. latipunctata males actually copulate with Amazon mollies, despite a pronounced preference for conspecific females. In laboratory experiments P. latipunctata males are capable of triggering embryogenesis in P. formosa females. Field observations support the hypothesis that P. latipunctata is a third host species for P. formosa, indicating that the Amazon molly effectively exploits all available host species for its gynogenetic mode of reproduction. Electronic Publication     

ORIGIN AND MAINTENANCE OF A FEMALE MATING PREFERENCE

We investigated the role of maintenance and origin of female mating preferences in three species of fish. Poecilia latipinna and P. mexicana are sexual species that hybridized to form the gynogenetic clonal P. formosa, which reproduces asexually but requires sperm to initiate embryogenesis. We demonstrate that all three species display almost identical and statistically indistinguishable preferences for large males. Although processes of good genes, runaway sexual selection, and direct selection could maintain preferences in the sexual species, good genes and runaway sexual selection are unlikely to operate in the asexual species. Furthermore, we found that the most likely direct selection benefit, an increase in fecundity, can also be excluded in the gynogens. We conclude that the most parsimonious explanation for this P. formosa preference is that it was inherited from the parental species and is maintained without forces generated by good genes, runaway selection, or direct selection for increased fecundity. This preference may be maintained because of pleiotropic effects (e.g., sensory bias) or mate searching costs.     

Divergent female mating preference in a clonal fish

In asexual all-female species, such as the Amazon molly, Poecilia formosa, that depend on sperm from “host males” only to trigger embryogenesis, mate choice does not provide any indirect, genetic benefits to the choosing female, although direct benefits are possible. Asexual species are thought to have a low evolutionary potential or evolvability due to the absence of meiotic recombination. Hence, theory predicts that mating preferences in P. formosa for male ornaments—if existent—should resemble those of females of the two parental species (Poecilia latipinna and Poecilia mexicana) involved in the natural hybridization that gave rise to the asexual P. formosa. When examining the female preference for dummy males with or without black vertical bars in the two parental species and in two lineages of P. formosa, a preference was detected in P. latipinna, but not in P. mexicana females. Interestingly, P. formosa living syntopic with P. latipinna also preferred striped males, while others living syntopic with P. mexicana preferred non-striped males. The evolutionary significance of this phenomenon remains largely unexplained, but it might indicate the evolution of mating preferences in a species with low evolutionary potential. Possible mechanisms include introgression and mitotic gene conversion. Females might use male coloration as indicator mechanisms for male traits that matter in terms of direct benefits.     

Character displacement in sailfin mollies, <Emphasis Type="Italic">Poecilia latipinna</Emphasis>: allozymes and behavior

Synopsis We analyzed variation in allozymes and mating preferences in 12 populations across much of the range of the sailfin molly, Poecilia latipinna. Sailfin mollies can be sympatric with its sexual parasite Amazon mollies, P. formosa. Amazon mollies must co-exist and mate with bisexual males of closely related species (including sailfin mollies) to induce embryogenesis but inheritance is strictly maternal. Where sailfin and Amazon mollies are sympatric there is evidence of reproductive character displacement as males show a significantly stronger mating preference for sailfin molly females over Amazon mollies compared to preferences of males from allopatric populations. From the allozyme data we found a moderate amount of genetic variation across all populations but this variation did not reveal significant partitioning between sympatric and allopatric populations. Additionally, we found no evidence for isolation by distance as genetic distance was not significantly correlated with geographic distance. While allozyme variation also did not significantly correlate with male mating preferences, there was a significant correlation between male mating preferences and geographic distance. This correlation between mating preferences and geographic distance may have arisen from coevolution with Amazon mollies resulting in reproductive character displacement. Taken together, the distribution of genetic and behavioral variation among sympatric and allopatric populations suggests that behavioral evolution has outpaced evolution at the allozyme loci we examined in P. latipinna.     

Male Sailfin mollies (Poecilia latipinna) copy the mate choice of other males

Female mate-copying has been shown to occur between heterospecifics:female sailfin mollies Poecilia latipinna copy the choice oftheir gynogenetic associates, Amazon mollies P. formosa. Femalemate-copying thus contributes to the maintenance of this asexual-sexualspecies complex by providing an advantage to male sailfin molliesthat mate with Amazon females; because of mate-copying thesemales increase their attractiveness to conspecific females.Here we show that male mate-copying, an unreported phenomenon,also occurs and that it can reverse male preferences for conspecificfemales. Male mate-copying should also contribute to the maintenanceof gynogens and might be advantageous in allowing males a meansto rapidly assess female receptivity although sometimes resultingin heterospedfic matings.     

Are you more than the sum of your parents’ genes? Phenotypic plasticity in a clonal vertebrate and F1 hybrids of its parental species

All known vertebrate clones have originated from hybridization events and some have produced distinct evolutionary lineages via hybrid speciation. Amazon mollies (Poecilia formosa) present an excellent study system to investigate how clonal species have adapted to heterogeneous environments because they are the product of a single hybridization event between male sailfin mollies (Poecilia latipinna) and female Atlantic mollies (Poecilia mexicana). Here, we ask whether the hybrid species differs from the combination of its parental species’ genes in its plastic response to different environments. Using a three-way factorial design, we exposed neonates produced by Amazon mollies and reciprocal F1 hybrid crosses to different thermal (24°C and 29°C) and salinity (0/2, 12, and 20 ppt) regimes. We measured various ontogenetic and life history characteristics across the life span of females. Our major results were as follows: (1) Reaction norms of growth and maturation to temperature and salinity are quite similar between the two hybrid crosses; (2) Amazon molly reaction norms were qualitatively different than the P. latipinna male and P. mexicana female (L×M) hybrids for the ontogenetic variables; (3) Amazon molly reaction norms in reproductive traits were also quite different from L×M hybrids; and (4) The reaction norms of net fertility were very different between Amazon mollies and L×M hybrids. We conclude that best locale for Amazon mollies is not the best locale for hybrids, which suggests that Amazon mollies are not just an unmodified mix of parental genes but instead have adapted to the variable environments in which they are found. Hybridization resulting in asexuality may represent an underappreciated mechanism of speciation because the unlikely events required to produce such hybrids rarely occur and is dependent upon the genetic distance between parental species.     

Independent Mating Preferences for Male Body Size and Coloration in Female Trinidadian Guppies

Although females in numerous species generally prefer males with larger, brighter and more elaborate sexual traits, there is nonetheless considerable intra‐ and interpopulation variation in mating preferences amongst females that requires explanation. Such variation exists in the Trinidadian guppy, Poecilia reticulata, an important model organism for the study of sexual selection and mate choice. While female guppies tend to prefer more ornamented males as mates, particularly those with greater amounts of orange coloration, there remains variation both in male traits and female mating preferences within and between populations. Male body size is another trait that is sexually selected through female mate choice in some species, but has not been examined as extensively as body coloration in the guppy despite known intra‐ and interpopulation variation in this trait among adult males and its importance for survivorship in this species. In this study, we used a dichotomous‐choice test to quantify the mating preferences of female guppies, originating from a low‐predation population in Trinidad, for two male traits, body length and area of the body covered with orange and black pigmentation, independently of each other. We expected strong female mating preferences for both male body length and coloration in this population, given relaxation from predation and presumably relatively low cost of choice. Females indeed exhibited a strong preference for larger males as expected, but surprisingly a weaker (but nonetheless significant) preference for orange and black coloration. Interestingly, larger females demonstrated stronger preferences for larger males than did smaller females, which could potentially lead to size‐assortative mating in nature.     

Reproductive interference by male Drosophila subobscura on female D. persimilis: A laboratory experiment

While females often reject courtship attempts by heterospecific males, reproductive interference by harassment from such males can nonetheless occur, potentially reducing female fitness. Such effects may be profound following a range expansion, when males from a new species may suddenly encounter (and perhaps even become abundant relative to) females of related native species. Drosophila subobscura recently invaded North America and may impact native species through reproductive interference and other processes. We test for the potential for reproductive interference by D. subobscura males on D. persimilis females in the laboratory. D. subobscura males aggressively copulated with D. persimilis females, including many females that exhibit rejection behaviors. Despite females attempting to dismount the males, the heterospecific copulations are on average longer than conspecific copulations, and females exhibit some reluctance to remate with conspecific males following this harassment. Females confined with both conspecific and heterospecific males produce fewer adult progeny than those with either conspecific males only or with conspecific males and distantly related D. simulans males that do not engage in female harassment. Overall, our results illustrate how reproductive interference by an invasive species can have negative effects on resident natural populations.     

Independent evolution of sexual dimorphism and female‐limited mimicry in swallowtail butterflies (Papilio dardanus and Papilio phorcas)

Several species of swallowtail butterflies (genus Papilio) are Batesian mimics that express multiple mimetic female forms, while the males are monomorphic and nonmimetic. The evolution of such sex‐limited mimicry may involve sexual dimorphism arising first and mimicry subsequently. Such a stepwise scenario through a nonmimetic, sexually dimorphic stage has been proposed for two closely related sexually dimorphic species: Papilio phorcas, a nonmimetic species with two female forms, and Papilio dardanus, a female‐limited polymorphic mimetic species. Their close relationship indicates that female‐limited polymorphism could be a shared derived character of the two species. Here, we present a phylogenomic analysis of the dardanus group using 3964 nuclear loci and whole mitochondrial genomes, showing that they are not sister species and thus that the sexually dimorphic state has arisen independently in the two species. Nonhomology of the female polymorphism in both species is supported by population genetic analysis of engrailed, the presumed mimicry switch locus in P. dardanus. McDonald–Kreitman tests performed on SNPs in engrailed showed the signature of balancing selection in a polymorphic population of P. dardanus, but not in monomorphic populations, nor in the nonmimetic P. phorcas. Hence, the wing polymorphism does not balance polymorphisms in engrailed in P. phorcas. Equally, unlike in P. dardanus, none of the SNPs in P. phorcas engrailed were associated with either female morph. We conclude that sexual dimorphism due to female polymorphism evolved independently in both species from monomorphic, nonmimetic states. While sexual selection may drive male–female dimorphism in nonmimetic species, in mimetic Papilios, natural selection for protection from predators in females is an alternative route to sexual dimorphism.     

New microsatellite loci confirm hybrid origin,parthenogenetic inheritance,and mitotic gene conversion in the gynogenetic Amazon molly (Poecilia formosa)

We describe the first microsatellite loci for the gynogenetic Amazon molly, Poecilia formosa, an all‐female species arisen through hybridization of the bisexual species Poecilia mexicana and Poecilia latipinna. The loci showed one to six alleles and an expected heterozygosity between zero and 0.75. As expected with parthenogenetic inheritance, most loci were either constantly homozygous (five loci) or constantly heterozygous (eight loci). For six loci, both heterozygotes and homozygotes occurred. This and the fact that some loci only showed alleles of one of the ancestral species could indicate genome homogenization through mitotic gene conversion. Our new loci conformed to the hybrid origin of Amazon molly and are also applicable to both ancestral bisexual species.     

Effects of algal food quality on sexual reproduction of Daphnia magna

The objective of our study was to investigate sexual reproduction of Daphnia magna associated with mating behaviors and hatching rates, according to different algal food sources. Since a diatom is known to contain more abundant long‐chain poly unsaturated fatty acids (PUFAs), we hypothesized that the diatom‐consuming D. magna would exhibit more successful reproduction rates. Upon the hypothesis, we designed three experiments using two algal species, a green alga (Chlorella vulgaris) and a diatom (Stephanodiscus hantzschii). From the results, we found that the mating frequency and copulation duration increased in the treatment with S. hantzschii, resulting in a significant increase of hatching rates of resting eggs. In the other two repetitive mating strategies (e.g., one female vs. multiple males, and one male vs. multiple females), we found that the hatching rates of resting eggs were greater in the S. hantzschii treatment. In addition to the mating strategy, male body size significantly increased in the diatom treatment, hence average diameter of penis was also statistically different among the treatments (greater diameter in the S. hantzschii treatment). To examine the effect of algal food quality, we estimated quantity of fatty acids in the two algal species. Our result showed that S. hantzschii had a higher proportion of long‐chain PUFAs than C. vulgaris. Furthermore, a stable isotope analysis revealed that carbon and nitrogen originated from S. hantzschii were more assimilated to D. magna. In summary, our study manifested that diatom consumption of D. magna leads to more successful sexual reproduction. We then discussed how the diatom consumption of zooplankton influences food web dynamics in a freshwater ecosystem.     

An atypical reproductive cycle in a common viviparous Asia Agamid Phrynocephalus vlangalii

Viviparous lizards living in cold climate of high altitude often exhibit atypical reproductive cycles, in which mating and fertilization occur synchronously and annually with parturition occurring at the end of the year. Nevertheless, detailed case studies on atypical reproductive cycles are few. Using anatomical data combined with behavioral observations, we examined the reproductive cycle of a common Asian agamid, Phrynocephalus vlangalii, from a high‐elevation area in Sichuan, China. Male spermiation of P. vlangalii occurred in May, and spermatogenesis began in June and reached a maximum in October. For females, ovulation and fertilization occurred in May, and females developed gestation and pregnancy in 3 months from June to August, without vitellogenesis during this period. Females gave birth synchronously in late August, then vitellogenesis began and lasted until May of the next year. All adult males and females were synchronized in the same reproductive condition each month. The synchronous and annual reproductive cycle of P. vlangalii clearly represents an atypical cycle. The male courtship and mating behaviors were concordant with gonadal cycle and mainly happened in May and June. Despite the short growth period for neonates, they had a high over‐winter survival rate of 84.4%, suggesting that autumn parturition did not generate high costs to this reproductive cycle. We propose that the high over‐winter survival rate of neonates is likely linked with female delayed sexual maturity, female asynchronous vitellogenesis and gestation, large relative clutch mass (RCM), and adult‐offspring burrow sharing behavior during hibernation.     

Mode of hybridogenesis and habitat preferences influence population composition of water frogs (Pelophylax esculentus complex,Anura: Ranidae) in a region of sympatric occurrence (western Slovakia)

Coexistence of sperm‐dependent asexual hybrids with their sexual progenitors depends on genetic and ecological interactions between sexual and asexual forms. In this study, we investigate genotypic composition, modes of hybridogenetic gametogenesis and habitat preferences of European water frogs (Pelophylax esculentus complex) in a region of sympatric occurrence. Pelophylax esculentus complex comprises parental species P. ridibundus and P. lessonae, whose primary hybridization leads to hybridogenetic lineages of P. esculentus. Hybrids clonally transmit one parental genome and mate with the other parental species, forming a new generation of hybrids. In the region of western Slovakia, we found syntopic occurrence of diploid and triploid hybrids with P. lessonae, syntopic occurrence of all three taxa as well as the existence of pure P. ridibundus populations. All triploid hybrids were exclusively male possessing one ridibundus and two different lessonae genomes (RLL). Sex ratio in diploid hybrids was substantially female‐biased. Irrespective of the population composition, diploid hybrids excluded the lessonae genome from their germ line and produced ridibundus gametes. Contrarily, RLL males unequivocally eliminated the ridibundus genome and produced diploid lessonae sperms. Perpetuation of RLL males in studied populations is most likely achieved by their mating with diploid hybrid females. The composition of water frog populations is also shaped by taxon‐specific habitat preferences. While P. ridibundus preferred larger water bodies (gravelpits, fishery ponds, dead river arms), P. lessonae was most frequently found in marshes and smaller sandpits. Pelophylax esculentus occupied predominately similar habitats as its sexual host P. lessonae.     

Absence of Mate Choice and Postcopulatory Benefits in a Species with Extreme Sexual Size Dimorphism

Most hypotheses related to the evolution of female‐biased extreme sexual size dimorphism (SSD) attribute the differences in the size of each sex to selection for reproduction, either through selection for increased female fecundity or selection for male increased mobility and faster development. Very few studies, however, have tested for direct fitness benefits associated with the latter – small male size. Mecaphesa celer is a crab spider with extreme SSD, whose males are less than half the size of females and often weigh 10 times less. Here, we test the hypotheses that larger size in females and smaller size in males are sexually selected through differential pre‐ and postcopulatory reproductive benefits. To do so, we tested the following predictions: matings between small males and large females are more likely to occur due to mate choice; females mated to small males are less likely to accept second copulation attempts; and matings between small males and large females will result in larger clutches of longer‐lived offspring. Following staged mating trials in the laboratory, we found no support for any of our predictions, suggesting that SSD in M. celer may not be driven by pre‐ or post‐reproductive fitness benefits to small males.     

The role of functional constraints in nonrandom mating patterns for a dance fly with female ornaments

Most hypotheses to explain nonrandom mating patterns invoke mate choice, particularly in species that display elaborate ornaments. However, conflicting selection pressures on traits can result in functional constraints that can also cause nonrandom mating patterns. We tested for functional load‐lifting constraints during aerial copulation in Rhamphomyia longicauda, a species of dance fly that displays multiple extravagant female‐specific ornaments that are unusual among sexual traits because they are under stabilizing selection. R. longicauda males provide females with a nuptial gift before engaging in aerial mating, and the male bears the entire weight of the female and nuptial gift for the duration of copulation. In theory, a male's ability to carry females and nuptial gifts could constrain pairing opportunities for the heaviest females, as reported for nonornamented dance flies. In concert with directional preferences for large females with mature eggs, such a load‐lifting constraint could produce the stabilizing selection on female size previously observed in this species. We therefore tested whether wild‐caught male R. longicauda collected during copulation were experiencing load‐lift limitations by comparing the mass carried by males during copulation with the male's wing loading traits. We also performed permutation tests to determine whether the loads carried by males during copulation were lighter than expected. We found that heavier males are more often found mating with heavier females suggesting that whereas R. longicauda males do not experience a load‐lift constraint, there is a strong relationship of assortative mating by mass. We suggest that active male mate choice for intermediately adorned females is more likely to be causing the nonrandom mating patterns observed in R. longicauda.     

Phylogenetic Position of Parasitic Chytrids on Diatoms: Characterization of a Novel Clade in Chytridiomycota

Chytrids are true fungi that reproduce with posteriorly uniflagellate zoospores. In the last decade, environmental DNA surveys revealed a large number of uncultured chytrids as well as undescribed order‐level novel clades in Chytridiomycota. Although many species have been morphologically described, only some DNA sequence data of parasitic chytrids are available from the database. We herein discuss five cultures of parasitic chytrids on diatoms Aulacoseira spp. and Asterionella formosa. In order to identify the chytrids examined, thallus morphologies were observed using light microscopy. We also conducted a phylogenetic analysis using 18S, 5.8S, and 28S rDNA sequences to obtain their phylogenetic positions. Based on their morphological characteristics, two cultures parasitic on As. formosa were identified as Rhizophydium planktonicum and Zygorhizidium planktonicum. The other three cultures infecting Aulacoseira spp. (two on Aulacoseira ambigua and the other on Aulacoseira granulata) were regarded as Zygorhizidium aff. melosirae. The results of the molecular phylogenetic analysis revealed that R. planktonicum belonged to the known order Chytridiales, while the two species of Zygorhizidium were placed in a novel clade that was previously reported as an undescribed clade composed of only the environmental sequences of uncultured chytrids.