Climate-driven Population Differentiation And Adaptive Evolution Studies In Spotted Sea Bass And Large Yellow Croaker

Global climate change leads to a series of changes such as rising of sea level,ocean acidification,and increasing frequency of extreme whether events etc.These changes not only pose decisive impacts on growth,development,and behaviors of marine fishes,but also greatly influence their reproduction,population size,and distribution at population level.In a larger timescale,these influences will ultimately determine the progress and destiny of population differentiation and evolution in marine fishes.Chinese marginal seas are famous because their unique geographic structure and complex hydrological characteristics,such as wide latitudinal range,various environments,and fragmented topography.These characteristics may impede the communication of genetic materials between different local populations in marine fishes,and provide the possibility of the formation of structured and complex population systems.Therefore,Chinese marginal seas constitute an ideal marine environment system for climatic adaptation and evolution studies in marine fishes.The spotted sea bass(Lateolabrax maculatus)and large yellow croaker(Larimichthys crocea)belong to Perciformes.They both are at pivotal positions in Chinese mariculture industry due to their highest yields and economic values among fish species.Meanwhile,they have some differences in their physiological characteristics and reproductive behaviors.The spotted sea bas is a classic eurythermal fish inhabit in a broad latitudinal range.But their dispersal abilities are limited.However,the large yellow croaker has a narrower tolerable-temperature range and a much stronger dispersal ability.By investigating and comparing their population structure and genome-wide selective signatures,we can make a great progress in understanding the population differentiation patterns and adaptive evolution mechanism under the impacts of global climate changes in marine fishes.Besides,taking the advantages of fast development of sequencing and bioinformatic technologies,population genetics and evolutionary biology have evolved new research core methods and contents in recent years.Based on all above,we collected spotted sea basses and large yellow croakers along the whole Chinese coastlines,assembled new reference genomes,and discovered millions of genome-wide polymorphism genetic markers.Then conducted modern population genetic and evolutionary biology studies using these markers to elucidate the patterns and mechanisms of population differentiation and adaptive evolution under the impacts of global climate changes in marine fishes.Specifically,the main results and conclusions are as follows:(1)Chromosome-level assembly of the spotted sea bassWe de novo assembled a chromosome-level reference genome assembly of spotted sea bass,with a total size of 597.39Mbp and a N50 length of 182.31 Kbp and a scaffold N50 length of 2.79 Mbp.Besides,a total of 23,657 protein-coding genes have been predicted with average 9.75 exons per gene,of which 22,509 genes can be annotated with preliminary function.We also identified approximately 17.66%of L.maculatus genome as repeats including 6.09%DNA transposons,2.31%long terminal repeats(LTRs)and 4.99%long interspersed nuclear elements(LINEs).The highquality chromosome-level genome of L.maculatus provides a valuable genetic resource for population genetics,adaptive evolution,and genetic breeding of this ecologically and economically important teleost fish.(2)Population genetics and evolution history of the spotted sea bassSpotted sea bass has a broad latitudinal distribution range along the marginal seas of the Northwest Pacific,providing an excellent teleost model for population genetic and climate adaptation studies.However,it is still eager for high-quality genomic resources to detect selective signatures and explore driving forces of genetic differentiation in this species.We,therefore,generated over 8.57 million SNP loci using whole-genome re-sequencing from 100 samples collected at 14 geographic sites(five or ten samples per site).After built the phylogeographic structure and demographic history,we found that three highly-differentiated populations exist in this species.Within them,the northeast Bohai Gulf population is the most ancient one and the southeast Beibu Gulf population appears most recently.We also determined that both isolation-by-distance and isolation-by-environment patterns significantly impacted genetic divergence,indicating that random drift and natural selection shape the population structure of spotted sea bass.(3)Genetic mechanism of climate adaptation in the spotted sea bassTemperature is an important climatic factor that shapes the distribution of eurythermal species.The northmost habitat of spotted sea bass reaches 41°N in temperate Bohai Gulf and the southmost reaches at least 20°N in tropical Beibu Gulf.The very different environments of L.maculatus living in Bohai Gulf and Beibu Gulf make them divergent in genetic structures and phenotypes,which provides us with a feasible fish model for population genetic studies in continual marginal sea.Based on the genome-wide SNP markers and genetic structure,we scanned the genome-wide evolutionary signatures of climate adaptation identified many genes related to growth,muscle contraction,and the visual sense that suffered positive natural selection.Moreover,the contrasting pattern of natural selection between high-latitude populations and low-latitude populations prompted that the different strategies in trade-offs between growth rate and risk of mortality may play an essential role in adaptation to different local climates.(4)Chromosome-level assembly of the large yellow croakerWe report a chromosome-level reference genome of large yellow croaker(L.crocea)generated by employing the PacBio single molecule sequencing technique(SMRT)and high-throughput chromosome conformation capture(Hi-C)technologies.The genome sequences were assembled into 1,591 contigs with a total length of 723.86 Mbp and a contig N50 length of 2.83 Mbp.After chromosome-level scaffolding,24 scaffolds were constructed with a total length of 668.67 Mbp(92.48%of the total length).Genome annotation identified 23,657 protein-coding genes and 7262 ncRNAs.This highly accurate,chromosome-level reference genome of L.crocea provides an essential genome resource to support the development of genomescale selective breeding and restocking strategies of L.crocea.(5)Genetic structure and genome landscape of adaptive evolution in the large yellow croakerThe large yellow croaker,one of China’s most economically valuable marine fish.Because of the import implications for ecological protection,germplasm recovery,and fishery resource management,the debate about the stock division and distribution of this species lasted from the 1960s and remains until now.In 1960s,Tian and Xu et al.have promoted that there were three stocks,the Daiqu stock,Minyuedong stock and Naozhou stock.However,the wild germplasm resources have suffered a serious collapse of in past decades.The current population structure and habitat division have not been investigated in a fine-scale comprehensively.To address this,we built a finescale genetic structure of large yellow croaker populations distributed along the eastern and southern Chinese coastline based on 7.64 million SNP markers.Compared with the previous Daiqu-Minyuedong-Naozhou division system proposed in the 1960s,our results revealed a climate-driven habitat change probably occurred between the Naozhou(Nanhai)Stock and the Mingyuedong(Mindong)Stock.The boundary between these two stocks’ habitats might have shifted northwards from the Pearl River Estuary to the northern area of the Taiwan Strait,accompanied by highly asymmetric introgressions.In addition,we found two divergent landscapes of natural selection existed in different stocks living in north and south areas.The northern population suffered highly-gathered and strong natural selection around developmental-processrelated genes,which may help them exploit the rare growing periods efficiently.Meanwhile,we detected moderate and interspersed selective signatures from the southern populations.Moreover,many immune-related genes were associated with these signals,which aid in the adaptation to a high-pathogen-density warm environment.Overall,our studies on population genetics and evolutionary genomics in spotted sea basses and large yellow croakers reveal their patterns of differentiation and mechanisms underlying adaptive evolution.Owing similarities and differences in biology and genetics of these two species,they have divergent isolation patterns accompanied by commonalities in micro-evolution mechanisms adapting hot and cold environments,reflecting convergent evolution between them.These findings provide not only necessary basis on ecological protection of marine fishes living in Chinese coastal waters but also valuable inspiration and clues for further investigations in climatic adaptive evolution in marine teleost.