Sperm specificity and potential paternal effects in gynogenesis in the Amazon Molly (Poecilia formosa).

The Amazon Molly (Poecilia formosa) reproduces by gynogenesis, a relatively rare form of asexual reproduction where sperm is required to trigger embryogenesis, but male genes are not incorporated into the genome of the embryo. Studying gynogenesis could isolate paternal non-genetic effects on reproduction. This study explored which of eleven related species can produce sperm to trigger gynogenesis through natural mating in P. formosa, and whether sympatry affects reproductive success in P. formosa. Reproductive outcomes measured were relative reproductive output (number of offspring in the first brood divided by female standard length), relative embryo output (number of embryos in the first brood divided by female standard length) and combined relative reproductive output (sum of relative reproductive output and relative embryo output). For large (>4 cm) P. formosa, combined relative reproductive output was higher with sympatric Atlantic Molly (Poecilia mexicana) males than with allopatric P. mexicana males. P. formosa produced live offspring or late-stage embryos with all species tested in the genera Poecilia and Limia but did not produce offspring or embryos with males from the genera Gambusia, Girardinus, Heterandria, Poeciliopsis, or Xiphophorus. This information, as well as the limitations characterized in this study, will set a foundation for use of P. formosa as a model for paternal effects and the species specificity of sperm on fertilization, embryogenesis, and reproductive success.

Sperm-dependent asexual species and their role in ecology and evolution.

Sexual reproduction is the primary mode of reproduction in eukaryotes, but some organisms have evolved deviations from classical sex and switched to asexuality. These asexual lineages have sometimes been viewed as evolutionary dead ends, but recent research has revealed their importance in many areas of general biology. Our review explores the understudied, yet important mechanisms by which sperm-dependent asexuals that produce non-recombined gametes but rely on their fertilization, can have a significant impact on the evolution of coexisting sexual species and ecosystems. These impacts are concentrated around three major fields. Firstly, sperm-dependent asexuals can potentially impact the gene pool of coexisting sexual species by either restricting their population sizes or by providing bridges for interspecific gene flow whose type and consequences substantially differ from gene flow mechanisms expected under sexual reproduction. Secondly, they may impact on sexuals' diversification rates either directly, by serving as stepping-stones in speciation, or indirectly, by promoting the formation of pre- and postzygotic reproduction barriers among nascent species. Thirdly, they can potentially impact on spatial distribution of species, via direct or indirect (apparent) types of competition and Allee effects. For each such mechanism, we provide empirical examples of how natural sperm-dependent asexuals impact the evolution of their sexual counterparts. In particular, we highlight that these broad effects may last beyond the tenure of the individual asexual lineages causing them, which challenges the traditional perception that asexual lineages are short-lived evolutionary dead ends and minor sideshows. Our review also proposes new research directions to incorporate the aforementioned impacts of sperm-dependent asexuals. These research directions will ultimately enhance our understanding of the evolution of genomes and biological interactions in general.

Why do hybrids turn down sex?

Asexual reproduction is ancestral in prokaryotes; the switch to sexuality in eukaryotes is one of the major transitions in the history of life. The study of the maintenance of sex in eukaryotes has raised considerable interest for decades and is still one of evolutionary biology's most prominent question. The observation that many asexual species are of hybrid origin has led some to propose that asexuality in hybrids results from sexual processes being disturbed because of incompatibilities between the two parental species' genomes. However, in some cases, failure to produce asexual F1s in the lab may indicate that this mechanism is not the only road to asexuality in hybrid species. Here, we present a mathematical model and propose an alternative, adaptive route for the evolution of asexuality from previously sexual hybrids. Under some reproductive alterations, we show that asexuality can evolve to rescue hybrids' reproduction. Importantly, we highlight that when incompatibilities only affect the fusion of sperm and egg's genomes, the two traits that characterize asexuality, namely unreduced meiosis and the initiation of embryogenesis without the incorporation of the sperm's pronucleus, can evolve separately, greatly facilitating the overall evolutionary route. Taken together, our results provide an alternative, potentially complementary explanation for the link between asexuality and hybridization.

Male attention allocation depends on social context.

Allocation of attention, typically a limited capacity, is a mechanism used to filter large amounts of information and determine what stimuli are most relevant at a particular moment. In dynamic social environments as found in almost all species, including humans, multiple individuals may play a pivotal role in any given interaction where a male's attention may be divided between a rival, a current mate, and/or future potential mates. Although clearly important, the role of the social environment on attention in animals is not well understood. Here, we investigated impacts of the social environment on attention allocation using male sailfin mollies, Poecilia latipinna, which are a part of a sexual-unisexual mating system with the Amazon molly, Poecilia formosa. We asked: 1) Does the species of female influence the amount of attention a male allocates to her? And 2) Is a male's attention towards his mate influenced by different social partners? We show that males perceive a larger male as a more relevant stimulus to pay attention to compared to a smaller male, and a conspecific female (either a partner or audience) as a more relevant stimulus compared to a heterospecific female. Our results show that differential allocation of attention is dependent upon multiple components of the social environment in which an individual interacts. Understanding what qualities of rival males or potential mates provide enough meaning to males to cause a shift in attention away from a mating opportunity is essential to understanding the influence of the social environment in sexual selection.

Color polymorphism in the Cuban endemic livebearing fish Limia vittata (Teloestei, Poeciliidae): Potential roles of sexual and natural selection.

Color polymorphism can be maintained in natural populations by natural selection or sexual selection. In this study, we use two different approaches to test which of these evolutionary mechanisms may explain the presence of color polymorphism in the Cuban Limia (Limia vittata), an endemic livebearing fish from Cuba. First, we investigate the role of sexual selection using traditional binary choice tests looking at both female and male preferences relative to varying degrees of black spotting in stimulus mates. Second, we assess the role of natural selection by analyzing the frequency and geographic distribution of black-spotted and nonspotted morphs of L. vittata in natural populations from Cuba. The frequency of black-spotted morphs is significantly higher in brackish and saltwater environments compared with freshwater habitats, which could be related to higher predation pressure in coastal ecosystems compared with purely freshwater environments. Our results suggest that habitat variation is the most important factor in maintaining color polymorphism in L. vittata. Salinity levels could be indirectly responsible for maintaining different color morphs in this species, likely due to the regulatory effect of saline gradients on predation regimes.

A phylogeny of the genus Limia (Teleostei: Poeciliidae) suggests a single-lake radiation nested in a Caribbean-wide allopatric speciation scenario.

OBJECTIVE: The Caribbean is an important global biodiversity hotspot. Adaptive radiations there lead to many speciation events within a limited period and hence are particularly prominent biodiversity generators. A prime example are freshwater fish of the genus Limia, endemic to the Greater Antilles. Within Hispaniola, nine species have been described from a single isolated site, Lake Miragoâne, pointing towards extraordinary sympatric speciation. This study examines the evolutionary history of the Limia species in Lake Miragoâne, relative to their congeners throughout the Caribbean. RESULTS: For 12 Limia species, we obtained almost complete sequences of the mitochondrial cytochrome b gene, a well-established marker for lower-level taxonomic relationships. We included sequences of six further Limia species from GenBank (total N = 18 species). Our phylogenies are in concordance with other published phylogenies of Limia. There is strong support that the species found in Lake Miragoâne in Haiti are monophyletic, confirming a recent local radiation. Within Lake Miragoâne, speciation is likely extremely recent, leading to incomplete lineage sorting in the mtDNA. Future studies using multiple unlinked genetic markers are needed to disentangle the relationships within the Lake Miragoâne clade.

Biogeography of the West Indies: A complex scenario for species radiations in terrestrial and aquatic habitats.

Studies of the biogeography of the West Indies are numerous but not all taxonomic groups have received the same attention. Many of the contributions to this field have historically focused on terrestrial vertebrates from a perspective closely linked to the classical theory of island biogeography. However, some recent works have questioned whether some of the assumptions of this theory are too simplistic. In this review, we compiled information about the West Indies biogeography based on an extensive and rigorous literature search. While we offer some background of the main hypotheses that explain the origin of the Caribbean biota, our main purpose here is to highlight divergent diversification patterns observed in terrestrial versus aquatic groups of the West Indian biota and also to shed light on the unbalanced number of studies covering the biogeography of these groups of organisms. We use an objective method to compile existing information in the field and produce a rigorous literature review. Our results show that most of the relevant literature in the field is related to the study of terrestrial organisms (mainly vertebrates) and only a small portion covers aquatic groups. Specifically, livebearing fishes show interesting deviations from the species-area relationship predicted by classical island biogeography theory. We found that species richness on the Greater Antilles is positively correlated with island size but also with the presence of elevations showing that not only island area but also mountainous relief may be an important factor determining the number of freshwater species in the Greater Antilles. Our findings shed light on mechanisms that may differently drive speciation in aquatic versus terrestrial environments suggesting that ecological opportunity could outweigh the importance of island size in speciation. Investigations into freshwater fishes of the West Indies offer a promising avenue for understanding origins and subsequent diversification of the Caribbean biota.

Males can't afford to be choosy: Male reproductive investment does not influence preference for female size in Limia (Poeciliidae).

Reproductive investment was initially thought to be the key selective force behind male mate preference for female characters, like size or ornamentation (i.e., the preference by males for certain females). Yet, evidence of polygynous species, where male reproductive investments are often inexpensive compared to those of females, have also been described to possess male preference. Our study aims to understand how reproductive investment influences the selection of choosy males in polygynous systems using two species of livebearing fishes varying in reproductive investment: Limia perugiae, in which males invest heavily into reproduction, and L. zonata in which males invest minimally into reproduction. We hypothesized that male reproductive investment when combined with fecundity selection will favour the evolution of male mate preference and thereby lead to males that invest heavily into reproduction being choosier than males that invest minimally. When male Limia were exposed to two females simultaneously, one from the small size class and one from the large size class, L. zonata chose large females over small ones, whereas L. perugiae allocated the same amount of time regardless of female size class. Although we fail to find support for our original hypotheses, our study highlights the need for a more thorough examination of non-model species like Limia. We suggest future studies analyse reproductive investment as it interacts with cryptic choice, multiple sensory cues as well as expand comparisons to multiple Limia species, especially those endemic to Cuba, Grand Cayman, and Jamaica.

Male mate choice in livebearing fishes: an overview.

Although the majority of studies on mate choice focus on female mate choice, there is growing recognition of the role of male mate choice too. Male mate choice is tightly linked to 2 other phenomena: female competition for males and ornamentation in females. In the current article, I review the existing literature on this in a group of fishes, Poeciliidae. In this group, male mate choice appears to be based on differences in female quality, especially female size, which is a proxy for fecundity. Some males also have to choose between heterospecific and conspecific females in the unusual mating system of the Amazon molly. In this case, they typically show a preference for conspecific females. Whereas male mate choice is relatively well documented for this family, female ornamentation and female competition are not.

Male size, not female preferences influence female reproductive success in a poeciliid fish (Poecilia latipinna): a combined behavioural/genetic approach.

OBJECTIVE: We investigated the potential role of indirect benefits for female mate preferences in a highly promiscuous species of live-bearing fishes, the sailfin molly Poecilia latipinna using an integrative approach that combines methods from animal behavior, life-history evolution, and genetics. Males of this species solely contribute sperm for reproduction, and consequently females do not receive any direct benefits. Despite this, females typically show clear mate preferences. It has been suggested that females can increase their reproductive success through indirect benefits from choosing males of higher quality. RESULTS: Although preferences for large body size have been recorded as an honest signal for genetic quality, this particular study resulted in female preference being unaffected by male body size. Nonetheless, larger males did sire more offspring, but with no effect on offspring quality. This study presents a methodical innovation by combining preference testing with life history measurements-such as the determination of the dry weight of fish embryos-and paternity analyses on single fish embryos.

The role of mate-choice copying in speciation and hybridization.

Mate-choice copying, a social, non-genetic mechanism of mate choice, occurs when an individual (typically a female) copies the mate choice of other individuals via a process of social learning. Over the past 20 years, mate-choice copying has consistently been shown to affect mate choice in several species, by altering the genetically based expression of mating preferences. This behaviour has been claimed by several authors to have a significant role in evolution. Because it can cause or increase skews in male mating success, it seems to have the potential to induce a rapid change of the directionality and rate of sexual selection, possibly leading to divergent evolution and speciation. Theoretical work has, however, been challenging this view, showing that copying may decelerate sexual selection and that linkage disequilibrium cannot be established between the copied preference and the male trait, because females copy from unrelated individuals in the population, making an invasion of new and potentially fitter male traits difficult. Given this controversy, it is timely to ask about the real impact of mate-choice copying in speciation. We propose that a solution to this impasse may be the existence of some degree of habitat selection, which would create a spatial structure, causing scenarios of micro-allopatry and thus overcoming the problem of the lack of linkage disequilibrium. As far as we are aware, the potential role of mate-choice copying on fostering speciation in micro-allopatry has not been tackled. Also important is that the role of mate-choice copying has generally been discussed as being a barrier to gene flow. However, in our view, mate-choice copying may actually play a key role in facilitating gene flow, thereby fostering hybridization. Yet, the role of mate-choice copying in hybridization has so far been overlooked, although the conditions under which it might occur are more likely, or less restricted, than those favouring speciation. Hence, a conceptual framework is needed to identify the exact mechanisms and the conditions under which speciation or hybridization are expected. Here, we develop such a framework to be used as a roadmap for future research at the intersection of these research areas.

The gonadal transcriptome of the unisexual Amazon molly Poecilia formosa in comparison to its sexual ancestors, Poecilia mexicana and Poecilia latipinna.

BACKGROUND: The unisexual Amazon molly (Poecilia formosa) originated from a hybridization between two sexual species, the sailfin molly (Poecilia latipinna) and the Atlantic molly (Poecilia mexicana). The Amazon molly reproduces clonally via sperm-dependent parthenogenesis (gynogenesis), in which the sperm of closely related species triggers embryogenesis of the apomictic oocytes, but typically does not contribute genetic material to the next generation. We compare for the first time the gonadal transcriptome of the Amazon molly to those of both ancestral species, P. mexicana and P. latipinna. RESULTS: We sequenced the gonadal transcriptomes of the P. formosa and its parental species P. mexicana and P. latipinna using Illumina RNA-sequencing techniques (paired-end, 100 bp). De novo assembly of about 50 million raw read pairs for each species was performed using Trinity, yielding 106,922 transcripts for P. formosa, 115,175 for P. latipinna, and 133,025 for P. mexicana after eliminating contaminations. On the basis of sequence similarity comparisons to other teleost species and the UniProt databases, functional annotation, and differential expression analysis, we demonstrate the similarity of the transcriptomes among the three species. More than 40% of the transcripts for each species were functionally annotated and about 70% were assigned to orthologous genes of a closely related species. Differential expression analysis between the sexual and unisexual species uncovered 2035 up-regulated and 564 down-regulated genes in P. formosa. This was exemplary validated for six genes by qRT-PCR. CONCLUSIONS: We identified more than 130 genes related to meiosis and reproduction within the apomictically reproducing P. formosa. Overall expression of these genes seems to be down-regulated in the P. formosa transcriptome compared to both ancestral species (i.e., 106 genes down-regulated, 29 up-regulated). A further 35 meiosis and reproduction related genes were not found in the P. formosa transcriptome, but were only expressed in the sexual species. Our data support the hypothesis of general down-regulation of meiosis-related genes in the apomictic Amazon molly. Furthermore, the obtained dataset and identified gene catalog will serve as a resource for future research on the molecular mechanisms behind the reproductive mode of this unisexual species.

Allele-specific expression at the androgen receptor alpha gene in a hybrid unisexual fish, the Amazon molly (Poecilia formosa).

The all-female Amazon molly (Poecilia formosa) is the result of a hybridization of the Atlantic molly (P. mexicana) and the sailfin molly (P. latipinna) approximately 120,000 years ago. As a gynogenetic species, P. formosa needs to copulate with heterospecific males including males from one of its bisexual ancestral species. However, the sperm only triggers embryogenesis of the diploid eggs. The genetic information of the sperm donor typically will not contribute to the next generation of P. formosa. Hence, P. formosa possesses generally one allele from each of its ancestral species at any genetic locus. This raises the question whether both ancestral alleles are equally expressed in P. formosa. Allele-specific expression (ASE) has been previously assessed in various organisms, e.g., human and fish, and ASE was found to be important in the context of phenotypic variability and disease. In this study, we utilized Real-Time PCR techniques to estimate ASE of the androgen receptor alpha (arα) gene in several distinct tissues of Amazon mollies. We found an allelic bias favoring the maternal ancestor (P. mexicana) allele in ovarian tissue. This allelic bias was not observed in the gill or the brain tissue. Sequencing of the promoter regions of both alleles revealed an association between an Indel in a known CpG island and differential expression. Future studies may reveal whether our observed cis-regulatory divergence is caused by an ovary-specific trans-regulatory element, preferentially activating the allele of the maternal ancestor.

The Anthropocene Biosphere: Supporting 'Open Interdisciplinarity' through Blogging.

This paper describes a process of 'open' interdisciplinary scholarship. Researchers from across the University of Oklahoma blogged about a recent paper by ecologist Erle Ellis, and met in person to discuss posts. They then hosted Ellis for a seminar on questions that emerged, and for a public panel discussion.

Kin Recognition in a Clonal Fish, Poecilia formosa.

Relatedness strongly influences social behaviors in a wide variety of species. For most species, the highest typical degree of relatedness is between full siblings with 50% shared genes. However, this is poorly understood in species with unusually high relatedness between individuals: clonal organisms. Although there has been some investigation into clonal invertebrates and yeast, nothing is known about kin selection in clonal vertebrates. We show that a clonal fish, the Amazon molly (Poecilia formosa), can distinguish between different clonal lineages, associating with genetically identical, sister clones, and use multiple sensory modalities. Also, they scale their aggressive behaviors according to the relatedness to other females: they are more aggressive to non-related clones. Our results demonstrate that even in species with very small genetic differences between individuals, kin recognition can be adaptive. Their discriminatory abilities and regulation of costly behaviors provides a powerful example of natural selection in species with limited genetic diversity.

Sequence Evolution and Expression of the Androgen Receptor and Other Pathway-Related Genes in a Unisexual Fish, the Amazon Molly, Poecilia formosa, and Its Bisexual Ancestors.

The all-female Amazon molly (Poecilia formosa) originated from a single hybridization of two bisexual ancestors, Atlantic molly (Poecilia mexicana) and sailfin molly (Poecilia latipinna). As a gynogenetic species, the Amazon molly needs to copulate with a heterospecific male, but the genetic information of the sperm-donor does not contribute to the next generation, as the sperm only acts as the trigger for the diploid eggs' embryogenesis. Here, we study the sequence evolution and gene expression of the duplicated genes coding for androgen receptors (ars) and other pathway-related genes, i.e., the estrogen receptors (ers) and cytochrome P450, family19, subfamily A, aromatase genes (cyp19as), in the Amazon molly, in comparison to its bisexual ancestors. Mollies possess-as most other teleost fish-two copies of the ar, er, and cyp19a genes, i.e., arα/arß, erα/erß1, and cyp19a1 (also referred as cyp19a1a)/cyp19a2 (also referred to as cyp19a1b), respectively. Non-synonymous single nucleotide polymorphisms (SNPs) among the ancestral bisexual species were generally predicted not to alter protein function. Some derived substitutions in the P. mexicana and one in P. formosa are predicted to impact protein function. We also describe the gene expression pattern of the ars and pathway-related genes in various tissues (i.e., brain, gill, and ovary) and provide SNP markers for allele specific expression research. As a general tendency, the levels of gene expression were lowest in gill and highest in ovarian tissues, while expression levels in the brain were intermediate in most cases. Expression levels in P. formosa were conserved where expression did not differ between the two bisexual ancestors. In those cases where gene expression levels significantly differed between the bisexual species, P. formosa expression was always comparable to the higher expression level among the two ancestors. Interestingly, erß1 was expressed neither in brain nor in gill in the analyzed three molly species, which implies a more important role of erα in the estradiol synthesis pathway in these tissues. Furthermore, our data suggest that interactions of steroid-signaling pathway genes differ across tissues, in particular the interactions of ars and cyp19as.

Sex-specific local life-history adaptation in surface- and cave-dwelling Atlantic mollies (Poecilia mexicana).

Cavefishes have long been used as model organisms showcasing adaptive diversification, but does adaptation to caves also facilitate the evolution of reproductive isolation from surface ancestors? We raised offspring of wild-caught surface- and cave-dwelling ecotypes of the neotropical fish Poecilia mexicana to sexual maturity in a 12-month common garden experiment. Fish were raised under one of two food regimes (high vs. low), and this was crossed with differences in lighting conditions (permanent darkness vs. 12:12 h light:dark cycle) in a 2 × 2 factorial design, allowing us to elucidate potential patterns of local adaptation in life histories. Our results reveal a pattern of sex-specific local life-history adaptation: Surface molly females had the highest fitness in the treatment best resembling their habitat of origin (high food and a light:dark cycle), and suffered from almost complete reproductive failure in darkness, while cave molly females were not similarly affected in any treatment. Males of both ecotypes, on the other hand, showed only weak evidence for local adaptation. Nonetheless, local life-history adaptation in females likely contributes to ecological diversification in this system and other cave animals, further supporting the role of local adaptation due to strong divergent selection as a major force in ecological speciation.

Emergence of Leadership within a Homogeneous Group.

Large scale coordination without dominant, consistent leadership is frequent in nature. How individuals emerge from within the group as leaders, however transitory this position may be, has become an increasingly common question asked. This question is further complicated by the fact that in many of these aggregations, differences between individuals are minor and the group is largely considered to be homogeneous. In the simulations presented here, we investigate the emergence of leadership in the extreme situation in which all individuals are initially identical. Using a mathematical model developed using observations of natural systems, we show that the addition of a simple concept of leadership tendencies which is inspired by observations of natural systems and is affected by experience can produce distinct leaders and followers using a nonlinear feedback loop. Most importantly, our results show that small differences in experience can promote the rapid emergence of stable roles for leaders and followers. Our findings have implications for our understanding of adaptive behaviors in initially homogeneous groups, the role experience can play in shaping leadership tendencies, and the use of self-assessment in adapting behavior and, ultimately, self-role-assignment.

Comparative analysis of the gonadal transcriptomes of the all-female species Poecilia formosa and its maternal ancestor Poecilia mexicana.

BACKGROUND: The Amazon molly, Poecilia formosa (Teleostei: Poeciliinae) is an unisexual, all-female species. It evolved through the hybridisation of two closely related sexual species and exhibits clonal reproduction by sperm dependent parthenogenesis (or gynogenesis) where the sperm of a parental species is only used to activate embryogenesis of the apomictic, diploid eggs but does not contribute genetic material to the offspring.Here we provide and describe the first de novo assembled transcriptome of the Amazon molly in comparison with its maternal ancestor, the Atlantic molly Poecilia mexicana. The transcriptome data were produced through sequencing of single end libraries (100 bp) with the Illumina sequencing technique. RESULTS: 83,504,382 reads for the Amazon molly and 81,625,840 for the Atlantic molly were assembled into 127,283 and 78,961 contigs for the Amazon molly and the Atlantic molly, respectively. 63% resp. 57% of the contigs could be annotated with gene ontology terms after sequence similarity comparisons. Furthermore, we were able to identify genes normally involved in reproduction and especially in meiosis also in the transcriptome dataset of the apomictic reproducing Amazon molly. CONCLUSIONS: We assembled and annotated the transcriptome of a non-model organism, the Amazon molly, without a reference genome (de novo). The obtained dataset is a fundamental resource for future research in functional and expression analysis. Also, the presence of 30 meiosis-specific genes within a species where no meiosis is known to take place is remarkable and raises new questions for future research.