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Hybridization is a major source of evolutionary innovation. In plants, epigenetic mechanisms can help to stabilize hybrid genomes and contribute to reproductive isolation, but the relationship between genetic and epigenetic changes in animal hybrids is unclear. We analysed the relationship between genetic background and methylation patterns in natural hybrids of two genetically divergent fish species with different mating systems, Kryptolebias hermaphroditus (self-fertilizing) and K. ocellatus (outcrossing). Co-existing parental species displayed highly distinct genetic (SNPs) and methylation patterns (37,000 differentially methylated cytosines). Hybrids had predominantly intermediate methylation patterns (88.5% of the sites) suggesting additive effects, as expected from hybridization between genetically distant species. The large number of differentially methylated cytosines between hybrids and parental species (n = 5,800) suggests that hybridization may play a role in increasing genetic and epigenetic variation. Although most of the observed epigenetic variation was additive and had a strong genetic component, we also found a small percentage of non-additive, potentially stochastic, methylation differences that might act as an evolutionary bet-hedging strategy and increase fitness under environmental instability.

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Androdioecy, the coexistence of hermaphrodites and males, is very rare in vertebrates but occurs in mangrove killifish living in ephemeral or unstable habitats. Hermaphrodites reproduce both by outcrossing with males and by selfing. Outbreeding is advantageous because of inbreeding depression, but it requires encounters with males. The advantages of a propensity for outcrossing among hermaphrodites and the production of males affect each other very strongly. To study the evolutionary coupling of these two aspects, we here analyze a simple evolutionary game for a population composed of three phenotypes: outcrossing-oriented hermaphrodites, selfing-oriented hermaphrodites, and males. Outcrossing-oriented hermaphrodites first attempt to search for males and perform outcrossing if they encounter males. If they fail to encounter males, they reproduce via selfing. Selfing-oriented hermaphrodites simply reproduce by selfing. The replicator dynamics may show bistability, in which both the androdioecious population (with outcrossing-oriented hermaphrodites and males) and the pure hermaphroditic population are locally stable. The model shows the fraction of males is either zero or relatively high (more than 25%), which is not consistent with the observed low fraction of males (less than 5%). To explain this discrepancy, we studied several models including immigration and enforced copulation. We concluded that the observed pattern can be most likely explained by a population dominated by selfing-oriented hermaphrodites receiving immigration of males.

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Parental effects influence offspring phenotypes through pre- and post-natal routes but little is known about their molecular basis, and therefore their adaptive significance. Epigenetic modifications, which control gene expression without changes in the DNA sequence and are influenced by the environment, may contribute to parental effects. We investigated the effects of environmental enrichment on the behaviour, metabolic rate and brain DNA methylation patterns of parents and offspring of the highly inbreed mangrove killifish (Kryptolebias marmoratus). Parental fish reared in enriched environments had lower cortisol levels, lower metabolic rates and were more active and neophobic than those reared in barren environments. They also differed in 1,854 methylated cytosines (DMCs). Offspring activity and neophobia were determined by the parental environment. Among the DMCs of the parents, 98 followed the same methylation patterns in the offspring, three of which were significantly influenced by parental environments irrespective of their own rearing environment. Our results suggest that parental environment influences the behaviour and, to some extent, the brain DNA methylation patterns of the offspring.

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Parasite-mediated selection is one of the main drivers of genetic variation in natural populations. The persistence of long-term self-fertilization, however, challenges the notion that low genetic variation and inbreeding compromise the host's ability to respond to pathogens. DNA methylation represents a potential mechanism for generating additional adaptive variation under low genetic diversity. We compared genetic diversity (microsatellites and AFLPs), variation in DNA methylation (MS-AFLPs), and parasite loads in three populations of Kryptolebias hermaphroditus, a predomintanly self-fertilizing fish, to analyze the potential adaptive value of DNA methylation in relation to genetic diversity and parasite loads. We found strong genetic population structuring, as well as differences in parasite loads and methylation levels among sampling sites and selfing lineages. Globally, the interaction between parasites and inbreeding with selfing lineages influenced DNA methylation, but parasites seemed more important in determining methylation levels at the local scale.

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Epigenetic mechanisms generate plastic phenotypes that can become locally adapted across environments. Disentangling genomic from epigenomic variation is challenging in sexual species due to genetic variation among individuals, but it is easier in self-fertilizing species. We analysed DNA methylation patterns of two highly inbred strains of a naturally self-fertilizing fish reared in two contrasting environments to investigate the obligatory (genotype-dependent), facilitated (partially depend on the genotype) or pure (genotype-independent) nature of the epigenetic variation. We found higher methylation differentiation between genotypes than between environments. Most methylation differences between environments common to both strains followed a pattern where the two genotypes (inbred lines) responded to the same environmental context with contrasting DNA methylation levels (facilitated epialleles). Our findings suggest that, at least in part, DNA methylation could depend on the dynamic interaction between the genotype and the environment, which could explain the plasticity of epigenetically mediated phenotypes.

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The complete mitochondrial genome was sequenced from the mangrove killifish (Kryptolebias hermaphroditus). The genome sequence was 17,487 bp in size, and the gene order and contents were identical with those of the congeneric species (K. marmoratus) in the genus Kryptolebias with emphasis on the second control region (795 bp). Of 13 protein-coding genes (PGCs), 5 genes (ND2, CO2, CO3, ND3, and Cytb) had incomplete stop codons as shown in K. marmoratus. Furthermore, the stop codon of ND6 gene was AGG, while the start codon of CO1 gene was GTG. The base composition of K. hermaphroditus mitogenome showed an anti-G bias (13.45% and 8.19%) on the second and third position of the protein-coding genes (PCGs), respectively.

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During an ichthyological survey in September 2015 at the Ceará-Mirim River estuary, Rio Grande do Norte State, northeastern Brazil, we collected a male of Kryptolebias hermaphroditus , a cynolebiid species that had been previously described as containing exclusively self-fertilizing hermaphrodites. This is the first record of a male in this species, over 140 years after the discovery of the mangrove rivulid species from Brazil. Our discovery reinforces the need for more studies in K. hermaphroditus , as well as the potential of this species as a model for evolutionary studies due to its unique mating system.(AU)

Durante uma amostragem ictiológica em setembro de 2015 no estuário do rio Ceará-Mirim, Estado do Rio Grande do Norte, Nordeste do Brasil, nós coletamos um macho de Kryptolebias hermaphroditus , uma espécie de rivulídeo que foi descrita como contendo apenas hermafroditas auto-fertilizantes. Este é o primeiro registro de um macho dessa espécie, mais de 140 anos depois da descoberta das espécies de rivulídeos de manguezais do Brasil. Nossa descoberta reforça a necessidade de mais estudos em K . hermaphroditus , assim como, o potencial desta espécie como um modelo para estudos evolutivos devido ao seu sistema reprodutivo único.(AU)

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Self-fertilization (selfing) favours reproductive success when mate availability is low, but renders populations more vulnerable to environmental change by reducing genetic variability. A mixed-breeding strategy (alternating selfing and outcrossing) may allow species to balance these needs, but requires a system for regulating sexual identity. We explored the role of DNA methylation as a regulatory system for sex-ratio modulation in the mixed-mating fish Kryptolebias marmoratus. We found a significant interaction between sexual identity (male or hermaphrodite), temperature and methylation patterns when two selfing lines were exposed to different temperatures during development. We also identified several genes differentially methylated in males and hermaphrodites that represent candidates for the temperature-mediated sex regulation in K. marmoratus. We conclude that an epigenetic mechanism regulated by temperature modulates sexual identity in this selfing species, providing a potentially widespread mechanism by which environmental change may influence selfing rates. We also suggest that K. marmoratus, with naturally inbred populations, represents a good vertebrate model for epigenetic studies.

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