Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish

The establishment of reproductive barriers between populations can fuel the evolution of new species. A genetic framework for this process posits that “incompatible” interactions between genes can evolve that result in reduced survival or reproduction in hybrids. However, progress has been slow in identifying individual genes that underlie hybrid incompatibilities. We used a combination of approaches to map the genes that drive the development of an incompatibility that causes melanoma in swordtail fish hybrids. One of the genes involved in this incompatibility also causes melanoma in hybrids between distantly related species. Moreover, this melanoma reduces survival in the wild, likely because of progressive degradation of the fin. This work identifies genes underlying a vertebrate hybrid incompatibility and provides a glimpse into the action of these genes in natural hybrid populations.

Natural hybridization reveals incompatible alleles that cause melanoma in swordtail fish

The establishment of reproductive barriers between populations is the key process that fuels the evolution of new species. A genetic framework for this process was proposed over 80 years ago, which posits “incompatible” interactions between genes that result in reduced survival or reproduction in hybrids. Despite this foundational work, progress has been slow in identifying individual genes that underlie hybrid incompatibilities, with only a handful known to date. Here, we use a combination of approaches to precisely map the genes that drive the development of a melanoma incompatibility in swordtail fish hybrids. We find that one of the genes involved in this incompatibility also causes melanoma in hybrids between distantly related species. Moreover, we show that this melanoma reduces survival in the wild, likely due to progressive degradation of the fin. Together, this work represents only the second case where the genes underlying a vertebrate hybrid incompatibility have been identified and provides the first glimpse into the action of these genes in natural hybrid populations.One sentence summaryUsing a combination of mapping approaches, we identify interacting genes that lead to melanoma in hybrids and characterize their effects in natural hybrid populations.

Methylation pattern polymorphism of cyp19a in Nile tilapia and hybrids

Skewed sex development is prevalent in fish hybrids. However, the histological observation and molecular mechanisms remain elusive. In this study, we showed that the interspecific hybrids of the two fish species, Oreochromis niloticus and Oreochromis aureus, had a male ratio of 98.02%. Microscopic examination revealed that the gonads of both male and female hybrids were developmentally retarded. Compared with the ovaries, the testes of both O. niloticus and hybrids showed higher DNA methylation level in two selected regions in the promoter of cyp19a, the gonadal aromatase gene that converts androgens into estrogens, cyp19a showed higher level gene expression in the ovary than in the testis in both O. niloticus and hybrid tilapia. Methylation and gene expression level of cyp19a were negative correlation between the testis and ovary. Gene transcription was suppressed by the methylation of the cyp19a promoter in vitro. While there is no obvious difference of the methylation level in testis or ovary between O. niloticus and hybrids. Thus, the DNA methylation of the promoter of cyp19a may be an essential component of the sex maintenance, but not a determinant of high male ratio and developmental retardation of gonads in tilapia hybrids.

Chimeric Genes Revealed in the Polyploidy Fish Hybrids of Carassius cuvieri (Female) × Megalobrama amblycephala (Male)

The genomes of newly formed natural or artificial polyploids may experience rapid gene loss and genome restructuring. In this study, we obtained tetraploid hybrids (4n=148, 4nJB) and triploid hybrids (3n=124, 3nJB) derived from the hybridization of two different subfamily species Carassius cuvieri (♀, 2n = 100, JCC) and Megalobrama amblycephala (♂, 2n = 48, BSB). Some significant morphological and physiological differences were detected in the polyploidy hybrids compared with their parents. To reveal the molecular traits of the polyploids, we compared the liver transcriptomes of 4nJB, 3nJB and their parents. The results indicated high proportion chimeric genes (31 > %) and mutated orthologous genes (17 > %) both in 4nJB and 3nJB. We classified 10 gene patterns within three categories in 4nJB and 3nJB orthologous gene, and characterized 30 randomly chosen genes using genomic DNA to confirm the chimera or mutant. Moreover, we mapped chimeric genes involved pathways and discussed that the phenotypic novelty of the hybrids may relate to some chimeric genes. For example, we found there is an intragenic insertion in the K+ channel kcnk5b, which may be related to the novel presence of the barbels in 4nJB. Our results indicated that the genomes of newly formed polyploids experienced rapid restructuring post-polyploidization, which may results in the phenotypic and phenotypic changes among the polyploidy hybrid offspring. The formation of the 4nJB and 3nJB provided new insights into the genotypic and phenotypic diversity of hybrid fish resulting from distant hybridization between subfamilies.

Hybrid asexuality as a primary reproductive barrier: on the interconnection between asexuality and speciation

Speciation usually proceeds in a continuum from intensively hybridizing populations until the formation of irreversibly isolated species. Restriction of interspecific gene flow may often be achieved by gradual accumulation of intrinsic postzygotic incompatibilities with hybrid infertility typically evolving more rapidly than inviability. A reconstructed history of speciation in European loaches (Cobitis) reveals that accumulation of postzygotic reproductive incompatibilities may take an alternative, in the literature largely neglected, pathway through initiation of hybrids' asexuality rather than through a decrease in hybrids' fitness. Combined evidence shows that contemporary Cobitis species readily hybridize in hybrid zones, but their gene pools are isolated as hybridization produces infertile males and fertile but clonally reproducing females that cannot mediate introgressions. Nevertheless, coalescent analyses indicated intensive historical gene flow during earlier stages of Cobitis diversification, suggesting that non-clonal hybrids must have existed in the past. The revealed patterns imply that during the initial stages of speciation, hybridization between little diverged species produced recombinant hybrids mediating gene flow, but growing divergence among species caused disrupted meiosis in hybrids resulting in their clonality, which acts as a barrier to gene flow. Comparative analysis of published data on other fish hybrids corroborated the generality of our findings; the species pairs producing asexual hybrids were more genetically diverged than those pairs producing fertile sexual hybrids but less diverged than species pairs producing infertile hybrids. Hybrid asexuality therefore appears to evolve at lower divergence than other types of postzygotic barriers and might thus represent a primary reproductive barrier in many taxa.