UNISEXUAL/BISEXUAL BREEDING COMPLEXES IN POECILIIDAE: WHY DO MALES COPULATE WITH UNISEXUAL FEMALES?

Unisexual poeciliid fishes live as sexual parasites in breeding complexes with related bisexual species. Males of the host species copulate with unisexual females as well as with con-specifics, thus maintaining the unisexuals. Copulation with a unisexual offers no selective benefit for a male. A model is proposed that provides an explanation in terms of evolutionary ecology for why males copulate with unisexuals. It assumes that, before copulation, a male attempts to identify a female as conspecific or not but that the correctness of the identification depends on the length of time spent on the identification process. Some cost is involved in the passage of time, so an optimal time spent on identification must exist. Because subordinate males risk being driven away by dominant males, the optimal time is longer for males at the top of the dominance hierarchy than for males at the bottom. Such an optimal strategy gives a male the greatest possible average net benefit from a mating attempt, given his social status; this is a “best of a bad job” strategy.     

Reduction of competition between bisexual and unisexual females ofPoecilia in northeastern Mexico

Synopsis Breeding compexes of poeciliid fishes with a bisexual and two unisexual species were studied for mechanisms permitting Sympatric coexistence. The unisexuals are gynogenetic and thereby sexually dependent on the males of the bisexual species for sperm to initiate development, but inheritance is entirely maternal.Bisexual females are more abundant in headwater localities; unisexuals increase in downstream localities. Males were 10 – 18% of the total poeciliid population, regardless of the relative proportions of bisexual to unisexual females. Downstream localities were typified by greater habitat diversity, including a variety of backwater pools. The unisexuals showed a marked preference for such pools. Both field and laboratory studies showed that all three types of females as well as males preferred shaded areas with a gravel substrate.Although the four types of fish were found together, nearest neighbour data indicated that each type of female preferred its own kind. Males courted throughout the year and were indiscriminate in their choice of mates. Despite the skewed sex ratio, males were not in short supply because only a few females were sexually receptive at a given time. No significant differences existed between bisexuals and unisexuals in their relative reproductive outputs, but they were asynchronous.     

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.     

Sperm availability in naturally occurring bisexual-unisexual breeding complexes involvingPoecilia mexicana and the gynogenetic teleost,Poecilia formosa

Synopsis Testicular maturation indices (TMI) were determined for wild-caught males ofPoecilia mexicana by quantitative analysis of the frequency of ongoing stages of spermatogenesis and spermatid differentiation in sections of testes stained with the Feulgen reaction for DNA. In nature, males maintain essentially constant levels of sperm production throughout the year and show no significant variations in mean TMI values associated with season, microhabitat, standard body length, or rank in male dominance hierarchies. Winter males or males isolated from females in the laboratory show accumulation of mature spermatophores. These findings suggest that fluctuations in the microstructure of wild populations ofPoecilia from northeastern Mexico may be due primarily to differences in the temporal scheduling of female reproductive cycles and not to limitations imposed by sperm availability or male reproductive competence. The data are discussed in terms of competitive interactions within unisexual-bisexual breeding complexes involving the Amazon mollyP. formosa, its related triploid hybrids, and the bisexual species,P. mexicana.     

Aspects of the mating behaviour of male mollies (Poecilia spp.)

The unisexual fish Poecilia formosa (the Amazon molly) reproduces by gynogenesis, a process in which sperm from the males of the host bisexual species activates development of its eggs. Unisexuals live with one of the host species in nature and compete with bisexual females for the males. It was long thought that male discrimination and mate selection established a balance between the unisexual and bisexual populations. Thus, hierarchies of males were set up in which dominant males mated with their conspecific females and subordinates mated with the Amazon molly. Recent evidence suggested, however, that male fish do not discriminate between their own females and the Amazon molly, and that there always are more males available than sexually receptive females of both species.
Our findings indicate that male behaviour may be more complex than suggested by either hypothesis. Mate discrimination and courtship behaviour appear to increase with age, so that large males show almost complete preference for their conspecific females, but smaller males will mate with the Amazon molly. In complex groups, small males often dart in and mate with their own females whilst the large males are engaged in courtship activities and defence of territory.     

饲养条件下川金丝猴群中主雄的移除和替换对社群行为的影响

在上海野生动物园对一群半散养的川金丝猴进行了为期一年的行为学研究。在此期间,猴群中发生了4起家庭主雄被移除和替代事件和一个雌性群因繁殖需要引入一个成年雄猴的事件,该过程在饲养条件下首次被完整记录。观察发现,繁殖群中,在家庭主雄猴的健康状况良好期间,群中各雄性成员间的社会等级关系相当稳定,很少变动。主雄猴有效地控制着群体的秩序,并严格地看护着其家庭中的雌猴免受其他雄猴的侵扰,而且它也很少对其他低序位雄猴主动攻击。全雄群中则再由一个高序位雄猴控制其他低序位雄猴。疾病、衰老、前主雄猴的存在以及被饲养人员从群中移除进行治疗等都可能引起猴群社会发生很大动荡,尤其是全雄群中各雄猴的社会等级序位发生剧烈改变,甚至发生家庭主雄的替代。在本报道中,人为因素在主雄替代过程中起着主要作用。主雄替代一旦成功,新主雄会把原主雄赶入全雄群,攻击追撵其他低序位雄猴,并彻底与全雄群完全脱离。对于每一个新主雄,家庭中的雌猴对其的接纳表现出明显的选择倾向。雌性性选择可能是野生猴群中新家庭群建立一种内在基础机制,同时提示偷配发生的可能性。     

Paternity in wild ring‐tailed lemurs (Lemur catta): Implications for male mating strategies

In group‐living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single‐male monopolization of paternity in groups. Ring‐tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi‐male, multi‐female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra‐group males—posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80–95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra‐troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra‐group mating is a viable strategy that can result in extra‐group paternity for L. catta males.     

Cytological evidence for temporal differences during the asynchronous ovarian maturation of bisexual and unisexual fishes of the genus Poecilia

Comparisons based upon morphological features and cytochemical staining properties of chromatin, nucleoli, and the ooplasm were used in the present analysis of ovarian maturation in wild-caught Poecilia mexicana and its related gynogenetic diploid and triploid' species'. Using an empirically derived ovarian maturation index, seasonal and collection site differences were found between the unisexual and bisexual forms. These fish seem equally suited to their environments. However, our data indicate that differences in microhabitat can have a profound influence on oocyte development. Although females of Poecilia spp. have asynchronous cycles of ovarian maturation, we could not detect any peculiar cytological events associated with the gynogenetic mode of reproduction. Sperm were found in ovaries of both unisexual and bisexual forms indicating that the unisexuals can compete effectively with females of P. mexicana for matings with males of this species. The methods employed in this study provide a sensitive measure of reproductive potentials in sympatric species.     

Cryptic sex? Estimates of genome exchange in unisexual mole salamanders (Ambystoma sp.)

Cryptic sex has been argued to explain the exceptional longevity of certain parthenogenetic vertebrate lineages, yet direct measurements of genetic exchange between sexual and apparently parthenogenetic forms are rare. Female unisexual mole salamanders (Ambystoma sp.) are the oldest known unisexual vertebrate lineage (~5 million years), and one hypothesis for their persistence is that allopolyploid female unisexuals periodically exchange haploid genomes ‘genome exchange’ during gynogenetic reproduction with males from sympatric sexual species. We test this hypothesis by using genome‐specific microsatellite DNA markers to estimate the rates of genome exchange between sexual males and unisexual females in two ponds in NE Ohio. We also test the prediction that levels of gene flow should be higher for ‘sympatric’ (sexual males present) genomes in unisexuals compared to ‘allopatric’ (sexual males absent) unisexual genomes. We used a model testing framework in the coalescent‐based program MIGRATE‐N to compare models where unidirectional gene flow is present and absent between sexual species and unisexuals. As predicted, our results show higher levels of gene flow between sexuals and sympatric unisexual genomes compared to lower (likely artefactual) levels of gene flow between sexuals and allopatric unisexual genomes. Our results provide direct evidence that genome exchange between sexual and unisexual Ambystoma occurs and demonstrate that the magnitude depends on which sexual species are present. The relatively high levels of gene flow suggest that unisexuals must be at a selective advantage over sexual forms so as to avoid extinction due to genetic swamping through genome exchange.     

Dominance and Mating in a Communal Polygynandrous Bird: Cooperation or Indifference towards Mating Competitors?

The effect of dominance on the mating behaviour of both females and males was investigated for the communally breeding pukeko (Porphyrio porphyrio melanotus). Pukeko are polygynandrous with most groups consisting of three to 7 breeding males and one or two breeding females that lay eggs in a single nest. Linear dominance hierarchies are well established within breeding groups. Alpha females were involved in more copulations than beta females, but this difference did not appear to be a result of dominance status. There was also no evidence of egg tossing or egg destruction by breeding females. There was no positive correspondence between dominance rank of males and their frequency of sexual activity or copulations during the prelaying or laying periods. Dominants did interrupt matings by subordinates, but both qualitative and quantitative analyses of behaviour found no evidence of mate guarding. Furthermore dominants were no more likely to interrupt a copulation involving a subordinate male than they were to passively observe it or not react at all. This led us to suggest that males tended to behave indifferently toward mating competitors. As a result, multiple paternity is predicted to be high in pukeko groups. We also question the standard interpretation that males are behaving cooperatively in communal groups rather than coactively.     

Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes.

To persist, unisexual and asexual eukaryotes must have reproductive modes that circumvent normal bisexual reproduction. Parthenogenesis, gynogenesis, and hybridogenesis are the modes that have generally been ascribed to various unisexuals. Unisexual Ambystoma are abundant around the Great Lakes region of North America, and have variously been described as having all 3 reproductive modes. Diploid and polyploid unisexuals have nuclear genomes that combine the haploid genomes of 2 to 4 distinct sexual species, but the mtDNA is unlike any of those 4 species and is similar to another species, Ambystoma barbouri. To obtain better resolution of the reproductive mode used by unisexual Ambystoma and to explore the relationship of A. barbouri to the unisexuals, we sequenced the mitochondrial control and highly variable intergenic spacer region of 48 ambystomatids, which included 28 unisexuals, representatives of the 4 sexual species and A. barbouri. The unisexuals have similar sequences over most of their range, and form a close sister group to A. barbouri, with an estimated time of divergence of 2.4-3.9 million years ago. Individuals from the Lake Erie Islands (Kelleys, Pelee, North Bass) have a haplotype that demonstrates an isolation event. We examined highly variable microsatellite loci, and found that the genetic makeup of the unisexuals is highly variable and that unisexual individuals share microsatellite alleles with sexual individuals within populations. Although many progeny from the same female had the same genotype for 5 microsatellite DNA loci, there was no indication that any particular genome is consistently inherited in a clonal fashion in a population. The reproductive mode used by unisexual Ambystoma appears to be unique; we suggest kleptogenesis as a new unisexual reproductive mode that is used by these salamanders.     

Mate-Guarding as a Male Reproductive Tactic in <Emphasis Type="Italic">Propithecus verreauxi</Emphasis>

Sexual selection theory predicts that in group-living mammals, male reproductive tactics can lead to high reproductive skew in favor of dominant individuals. In sifakas (Propithecus verreauxi), a group-living primate with extremely seasonal reproduction, male reproductive success is highly skewed because dominant males sire almost all offspring despite a tendency toward an even adult group sex ratio. To understand the underlying behavioral mechanism resulting in this rank-related reproductive skew in male sifakas, we studied mate-guarding as a potential reproductive tactic. Behavioral observations of dominant males and adult females in combination with hormonal determination of timing of female receptivity in 9 groups at Kirindy Forest revealed that dominant males spent more time in proximity to females when they were receptive and were responsible for the maintenance of this proximity. Results also indicated that monopolization of receptive females was facilitated by both estrous asynchrony within groups and by the ability of dominant males to obtain olfactory cues as to the timing of female receptivity. Although dominant males engaging in mate-guarding are expected to experience various costs, there was no evidence for decreased foraging behavior and only a trend toward increased aggression between dominant and subordinate non-natal males within groups. Our results are in accordance with the hypothesis that dominant males use mate-guarding to monopolize receptive females and that it is one proximate mechanism that contributes to the high reproductive skew observed within the population of male sifakas at Kirindy.     

The role of female dominance hierarchies in the mating behaviour of mosquitofish

While studies of sexual selection focus primarily on female choice and male-male competition, males should also exert mate choice in order to maximize their reproductive success. We examined male mate choice in mosquitofish, Gambusia holbrooki, with respect to female size and female dominance. We found that the number of mating attempts made by a male was predicted by the dominance rank of females in a group, with dominant females attracting more mating attempts than subordinates. The number of mating attempts made by males was independent of the female size. The observed bias in the number of mating attempts towards dominant females may be driven either by straightforward male mate choice, since dominance and female fecundity are often closely related, or via the dominant females mediating male mating behaviour by restricting their access to subordinate females.     

MITOCHONDRIAL-DNA ANALYSES AND THE ORIGIN AND RELATIVE AGE OF PARTHENOGENETIC LIZARDS (GENUS CNEMIDOPHORUS). IV. NINE SEXLINEATUS-GROUP UNISEXUALS

Mitochondrial DNAs (mtDNAs) from nine morphologically distinct unisexual species and five bisexual species of lizards, all from the sexlineatus species-group of Cnemidophorus, were compared using restriction endonucleases. The unisexual lizards have mtDNAs that are identical at all or nearly all of the 128 sites cleaved. Although differing little in sequence, some mtDNAs differed in size due to the presence of tandem sequence duplications. Phylogenetic analysis of cleavage maps indicates that the mtDNAs of the unisexuals are most similar to that of the bisexual species C. inornatus. Considerable mtDNA diversity exists among C. inornatus populations, and one geographically restricted subspecies, C. i. arizonae, was identified as the most probable maternal ancestor of all nine unisexuals. All but one of these are triploid, and all have at least one C. inornatus gene complement. This, together with the homogeneity of their mtDNAs, suggests that all stem from one or a small number of allodiploid females (presumably parthenogenetic) that originated in a restricted geographic area in the recent past. These data, when combined with those from allozyme studies, preclude the possibility that most of the triploid unisexuals could have arisen via fertilization of an unreduced diploid ovum from one species by a haploid sperm from a different species.     

Special Adaptive Problems Associated with Unisexual Fishes

SYNOPSIS. Two genera of fishes, Poecilia and Poeciliopsis, bothin the family Poeciliidae, have established unisexual populations.One "species," Poecilia formosa, is a diploid form that reliesupon sperm from Poecilia latipinna or P. mexicana to initiateparthenogenetic development (gynogenesis). Triploid individualsof P. formosa have also been discovered but the mode of reproductionand the significance of such fish to natural populations haveyet to be established. In the genus Poeciliopsis three gynogenetic triploids are known.Each is superimposed on a different bisexual host: Poeciliopsislucida, P. monacha or P. viriosa. Five diploid hybridogeneticformsalso have been identified. These are fertilized by either P.lucida, P. latidens, or P. occidentalis. In hybridogenetic forms,sperm actually feitilizes the egg. A hybrid with maternal andpaternal characters is produced, but only maternal genes aretransmitted through the egg to the next generation. Because of their sperm dependency, all unisexual fishes mustreside with at least one of the parental species. They areforcedto compete with them for sperm, space, and other limited resources.The ability to produce two females for every one that bisexualsproduce suggests that the unisexuals have the potential to winthis competition; but in so doing, they would lose their sexualsupport and eliminate themselves. A density-dependent mate selectionsystem plays a role in establishing a workable balance betweenthe competing elements. Unisexual forms of both Poecilia and Poeciliopsis are of hybridorigin. For most of them, the parental precursors and the proportionof genetic material that each contributed to the unisexual isknown. The various genomes that make up the unisexuals are adaptedto a variety of habitats. Once these genomes are combined ina unisexual hybrid, potential for adaptation to multiple nichesexists; this coupled with heterosis contributes greatly to thesuccess of gynogenetic and hybridogenetic fishes.     

Dominance and reproductive success in primates

Theoretical models of the relationship between competition and differential reproduction in primates share the premise that agonistic dominance hierarchies determine differential access to those limited resources which are essential to reproduction. In particular, the priority-of-access-to-estrous-female model is based on the postulate that high rank in males enhances reproductive success. Tests for a correlation between rank and reproductive success in males have produced mixed results. Problems in measuring male reproductive success and in conceptualizing dominance systems are implicated in the diversity of conclusions reached. Other attributes which affect reproductive success have been proposed, and alternative models of mating systems, based on the concepts of reproductive strategies, social skills, and life histories have also been developed. Studies of differential reproduction in female primates are fewer, but have the advantage over male studies of directly measuring infant production and offspring survival. Research on the relationship between rank and reproductive success in females has shown that under conditions of low resource availability, subordinate females sometimes suffer reduced fecundity and infant survival as a result of restricted access to food and water. Under conditions of social stress, low-ranking females may suffer from disruption of their reproductive cycles, resulting in lowered fecundity. Dominant females may also incur reproductive costs as well as benefits for their social position. Better insights into the relationship between dominance and reproduction are potentially offered by improved genetic paternity measures, new models of social and demographic processes, and the recent availability of life history data from field studies.     

非优势顺位雄性黄山短尾猴的交配策略

在多雄多雌、顺位决定交配机会、雄性偏斜繁殖的非人灵长类社会中,低顺位雄性为提高自己的繁殖成功率,通常采取多样的交配策略以获得较多的交配机会。对非优势顺位雄性交配策略的研究可以增加对灵长类社会性行为复杂性的理解,对于深入探讨动物的婚配制度及繁殖策略具有十分重要的科学意义。本研究采用目 标动物取样法和全事件记录法,在２０１２ 年９ －１２ 月（交配期）记录了安徽黄山短尾猴鱼鳞坑ＹＡ１ 群中４ 只成年雄性个体的交配及有关的行为。研究发现：（１）非优势顺位雄性个体在远离优势顺位雄性视野范围的交配频次和交配时间显著高于优势顺位视野范围内;（２）与优势顺位雄性个体相比,非优势顺位雄性的强行交配（forced copulation）和隐秘交配（clandestine copulation）比例较高;（３） 就交配对象而言,对成功生育的雌性个体,优势顺位雄性在选择交配对象时具有明显的倾向性,非优势顺位雄性在选择时倾向性不显著;对未生育的雌性,优势顺位雄性更倾向于选择没有生殖经历的亚成年雌性个体,非优势顺位雄性则倾向于选择处于哺乳后期的成年雌性个体;（４）在具体交配策略上,优势顺位雄性选择跟随（follow） 雌性,非优势顺位雄性则通过做鬼脸 （grimacing）和性追求（sexual chasing）直接获取交配机会。本研究结果表明黄山短尾猴中非优势雄性个体形成了多变的交配策略,更多采取强制性方式,以获得更多的交配机会,多数的交配都是机会性的。     

Asymmetric dominance and asymmetric mate choice oppose premating isolation after allopatric divergence

Assortative mating promotes reproductive isolation and allows allopatric speciation processes to continue in secondary contact. As mating patterns are determined by mate preferences and intrasexual competition, we investigated male–male competition and behavioral isolation in simulated secondary contact among allopatric populations. Three allopatric color morphs of the cichlid fish Tropheus were tested against each other. Dyadic male–male contests revealed dominance of red males over bluish and yellow‐blotch males. Reproductive isolation in the presence of male–male competition was assessed from genetic parentage in experimental ponds and was highly asymmetric among pairs of color morphs. Red females mated only with red males, whereas the other females performed variable degrees of heteromorphic mating. Discrepancies between mating patterns in ponds and female preferences in a competition‐free, two‐way choice paradigm suggested that the dominance of red males interfered with positive assortative mating of females of the subordinate morphs and provoked asymmetric hybridization. Between the nonred morphs, a significant excess of negative assortative mating by yellow‐blotch females with bluish males did not coincide with asymmetric dominance among males. Hence, both negative assortative mating preferences and interference of male–male competition with positive assortative preferences forestall premating isolation, the latter especially in environments unsupportive of competition‐driven spatial segregation.