Accurate species phylogenies are a prerequisite for all evolutionary research. Teleosts are the largest and most diversified group of extant vertebrates, but relationships among their three oldest extant lineages remain unresolved. On the basis of seven high-quality new genome assemblies in Elopomorpha (tarpons, eels), we revisited the topology of the deepest branches of the teleost phylogeny using independent gene sequence and chromosomal rearrangement phylogenomic approaches. These analyses converged to a single scenario that unambiguously places the Elopomorpha and Osteoglossomorpha (arapaima, elephantnose fish) in a monophyletic sister group to all other teleosts, i.e., the Clupeocephala lineage (zebrafish, medaka). This finding resolves more than 50 years of controversy on the evolutionary relationships of these lineages and highlights the power of combining different levels of genome-wide information to solve complex phylogenies.

Background: The Percidae family comprises many fish species of major importance for aquaculture and fisheries. Based on three new chromosome-scale assemblies inPerca fluviatilis,Perca schrenkii, andSander vitreusalong with additional percid fish reference genomes, we provide an evolutionary and comparative genomic analysis of their sex-determination systems.Results: We explored the fate of a duplicated anti-Mullerian hormone receptor type-2 gene (amhr2bY), previously suggested to be the master sex-determining (MSD) gene inP. flavescens. Phylogenetically related and structurally similar amhr2duplicates (amhr2b) were found inP. schrenkiiandSander lucioperca, potentially dating this duplication event to their last common ancestor around 19–27 Mya. InP. fluviatilisandS. vitreus, thisamhr2bduplicate has been likely lost while it was subject to amplification inS. lucioperca. Analyses of theamhr2blocus inP. schrenkiisuggest that this duplication could be also male-specific as it is inP. flavescens. InP. fluviatilis, a relatively small (100 kb) non-recombinant sex-determining region (SDR) was characterized on chromosome 18 using population-genomics approaches. This SDR is characterized by many male-specific single-nucleotide variations (SNVs) and no large duplication/insertion event, suggesting thatP. fluviatilishas a male heterogametic sex-determination system (XX/XY), generated by allelic diversification. This SDR contains six annotated genes, including three (c18h1orf198,hsdl1,tbc1d32) with higher expression in the testis than in the ovary.Conclusions: Together, our results provide a new example of the highly dynamic sex chromosome turnover in teleosts and provide new genomic resources for Percidae, including sex-genotyping tools for all three knownPercaspecies.

Hemiculter leucisclus, as a widely distributed freshwater fish in China, provides an interesting model to explore the impact of drainage evolution and geologic history in the Pleistocene on diversification patterns. We collected the mitochondrial cytochrome b (cytb) gene and the recombination activating gene 2 (RAG2) from 1,070 individuals from 59 sampling locations. Phylogenetic and population genetic approaches were used to describe the phylogeographic pattern and to test how the geological and climatic factors on diversification. The results suggested that there existed four sublineages of the H. leucisclus across six river systems, among which two sublineages, showing strongly indigenous characteristics, are constrained to particular geographical regions in China. The molecular data and ancestral states demonstrated that the H. leucisclus possibly originated from the Pearl River basin during the later Pliocene. The phylogeographic pattern in H. leucisclus appears to have been driven by palaeoenvironmental perturbations rather than anthropogenic translocations. The geographically constrained sublineages A in the middle and lower Pearl River basin and sublineage B in the upper Yangtze River basin deserves special protection.

The novel hybrid fish BTB, derived from crossing blunt snout bream (Megalobrama amblycephala, BSB) and topmouth culter (Culter alburnus, TC), exhibits markedly hypoxia tolerance in aquaculture. In this study, hypoxic treatment experiments confirmed that, comparing to its original parent BSB, the tolerance to low oxygen of BTB increased by 20.0%. Furthermore, a comparative analysis of the transcriptome and metabolome was performed using gill tissues from BTB exposed to normoxic and hypoxic conditions. Under hypoxic conditions, BTB displayed adaptive modifications in gill lamellae and hemocytes. Transcriptomic profiling identified 789 differentially expressed genes (DEGs), with 298 upregulated and 491 downregulated, enriched in pathways including apoptosis, NK cell-mediated cytotoxicity, MAPK/TNF/Toll-like receptor signaling, and HIF-1/FoXO signaling pathways. Twelve hypoxia-related candidate genes (egln3, im_7150988, znf395a, hif-1an, mknk2b, pck2, ero1a, igfbp-1a, vhl, bpifcl, egln1a, and ccna1) were screened and validated as potential contributors to hypoxia tolerance. Metabolomics analysis revealed a total of 108 differential metabolites (78 upregulated and 30 downregulated), predominantly linked to Arginine and proline metabolism, Ether lipid metabolism, Arachidonic acid metabolism, and Glycerophospholipid metabolism. Association analysis of transcriptomics and metabolomics revealed that the DEGs and DMs were enriched in the pathways of glycerophospholipid metabolism, ether lipid metabolism, arachidonic acid metabolism, and arginine and proline metabolism. In summary, BTB exhibited relatively high hypoxia tolerance, and 12 candidate genes related to hypoxia tolerance were identified. These findings laid a foundation for further investigation into the mechanisms of hypoxia tolerance improvement in hybrid fish.