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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.
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 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.
One possible mechanism for the (co-)evolution of seemingly novel male traits and female preferences for them is that males exploit pre-existing female biases, and livebearing fishes (Poeciliidae) have been at the forefront of this research for almost two decades. Here, using 13 poeciliid species from four different genera, we tested whether mustache-like rostral filaments found in males of some Mexican molly (Poecilia sphenops) populations could have evolved due to exploitation of a pre-existing female bias. While Mexican mollies were the only species with a significant female association preference for mustached males, we also did not find any species exhibiting significant aversion for mustached males; rather, variance in female preference scores was large throughout. For example, more than 25% of females spent twice as much time with the mustached male compared to the non-mustached male in most species, but even 31% of Mexican molly females spent more time near the non-mustached male. Hence, a comparison of the strength of preference was inconclusive. We discuss the possibility that the female preference of P. sphenops for mustached males could be due to a female pre-existing bias (sensu lato), even if population means were not significant for species other than P. sphenops. This highlights the importance of distinguishing between population means and individual preferences when interpreting mate choice, and thus, adds depth to the concept of mating preferences as a motor for evolutionary change.
Life history traits within species often vary among different habitats. We measured female fecundity in mollies (Poecilia mexicana) from a H2S-rich cave and from a neighbouring surface habitat, as well as in laboratory-reared individuals of both populations raised in either light or continuous darkness. Compared to conspecifics from surface habitats, cave-dwelling P. mexicana had reduced fecundity (adjusted for size) in the field. In the laboratory, the fecundity of surface mollies was higher in light than in darkness, whereas fecundity in the cave mollies was almost unaffected by the ambient light conditions. Our results suggest a heritable component to the reduction in fecundity in female cave mollies. Moreover, the reduced plasticity in fecundity of cave mollies in response to light conditions might be an example of genetic assimilation or channelling of a life history trait in a population invading a new environment.
We investigated whether female association preferences for males are influenced by black spot disease (BSD), a parasite induced change of the host phenotype. We compared three different species of fish: a gynogenetic hybrid species, Poecilia formosa (amazon molly) and two sexual species (Poecilia latipinna and Poecilia mexicana), which were involved in the natural hybridisation leading to the amazon molly. Contrary to their sexual relatives, asexual amazon mollies significantly avoided images of males infected with black spot disease. We propose that amazon molly females have direct fitness benefits from choosing healthy males. The adaptive significance of the preference for BSD-uninfected males in the asexual amazon molly is yet unclear but may involve avoidance of predation or parasite infection as well as increased sperm availability
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
The Mexican tetra Astyanax fasciatus has evolved a variety of more or less color- and eyeless cave populations. Here we examined the evolution of the female preference for large male body size within different populations of this species, either surface- or cave-dwelling. Given the choice between visual cues from a large and a small male, females from the surface form as well as females from an eyed cave form showed a strong preference for large males. When only non-visual cues were presented in darkness, the surface females did not prefer either males. Among the six cave populations studied, females of the eyed cave form and females of one of the five eyeless cave populations showed a preference for large males. Apparently, not all cave populations of Astyanax have evolved non-visual mating preferences. We discuss the role of selection by benefits of non-visual mate choice for the evolution of non-visual mating preferences
Atlantic mollies (Poecilia mexicana) inhabit a variety of surface habitats, but they also occur in a sulfur cave in southern Mexico. We examined male mate choice relative to female body size in the cave population and in the most closely related surface-dwelling population from a nearby river. Males from both populations were either light- or dark-reared and could choose between two differently sized females either on the basis of visual cues in light or on the basis of solely nonvisual cues in darkness. Sexual preferences were estimated from the degree of association. Cave molly males always showed a preference for the larger female, both in light and in darkness. Among the surface males, only light-reared males showed a preference in the visual cues test, but not in darkness. In a control experiment, we demonstrated that male association preferences directly translate into actual mating preferences. Apparently, using visual cues for mate choice is the ancestral state in this system, and using nonvisual cues has evolved as a novel trait in the cave population. We discuss the evolution of nonvisual male mate choice in the context of changed environmental conditions, namely the absence of light, hypoxia, and toxic hydrogen sulfide in the cave
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/arβ, erα/erβ1, 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, erβ1 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.