Genome and population sequencing of a chromosome-level genome assembly of the Chinese tapertail anchovy (Coilia nasus) provides novel insights into migratory adaptation

Abstract

Background Seasonal migration is one of the most spectacular events in nature; however, the molecular mechanisms related to this phenomenon have not been investigated in detail. The Chinese tapertail, or Japanese grenadier anchovy, Coilia nasus, is a valuable migratory fish of high economic importance and special migratory dimorphism (with certain individuals as non-migratory residents). Results In this study, an 870.0-Mb high-quality genome was assembled by the combination of Illumina and Pacific Biosciences sequencing. Approximately 812.1 Mb of scaffolds were linked to 24 chromosomes using a high-density genetic map from a family of 104 full siblings and their parents. In addition, population sequencing of 96 representative individuals from diverse areas along the putative migration path identified 150 candidate genes, which are mainly enriched in 3 Ca2+-related pathways. Based on integrative genomic and transcriptomic analyses, we determined that the 3 Ca2+-related pathways are critical for promotion of migratory adaption. A large number of molecular markers were also identified, which distinguished migratory individuals and non-migratory freshwater residents. Conclusions We assembled a chromosome-level genome for the Chinese tapertail anchovy. The genome provided a valuable genetic resource for understanding of migratory adaption and population genetics and will benefit the aquaculture and management of this economically important fish.

The Mitochondrial Markers Provide New Insights Into the Population Demographic History of Coilia nasus With Two Ecotypes (Anadromous and Freshwater)

“…Our results also showed that the presence of lineage A (freshwater individuals) occupied low frequencies of haplotypes in the low reaches of the Yangtze implied extremely limited gene flow existed between the anadromous group and freshwater group. Our result was also supported by the phylogenetic analysis of representative individuals clearly corresponding to the anadromous group and freshwater group of C. nasus based on the entire genome SNP set (Xu et al, 2020). The middle reaches of the Yangtze River harbors a large number of lakes with different sizes (e.g., Tianezhou, Poyang Lake, and Dongting Lake), which would support optimum living and spawning conditions (e.g., fresh water, water temperature (15∼27.5 • C), depth (0.5∼3.0 m), suitable current (0.057∼0.075 m/s), and abundant zooplankton required for spawning) for freshwater group of C. nasus.…”

“…The middle reaches of the Yangtze River harbors a large number of lakes with different sizes (e.g., Tianezhou, Poyang Lake, and Dongting Lake), which would support optimum living and spawning conditions (e.g., fresh water, water temperature (15∼27.5 • C), depth (0.5∼3.0 m), suitable current (0.057∼0.075 m/s), and abundant zooplankton required for spawning) for freshwater group of C. nasus. The optimum living and spawning conditions for freshwater group of C. nasus, especially high quality fresh water, gentle currents and abundant zooplankton, could not be found in the low reaches of the Yangtze River and the China coast (Xu et al, 2020). The effect of isolation (the middle reaches of the Yangtze River vs. the low reaches of the Yangtze River and the China coast) and adaptation to the new freshwater habitats of the middle reaches of the Yangtze River for C. nasus freshwater form might be responsible for the module of finitely asymmetric gene flow from freshwater to anadromous populations (Zhang, 2001;Schluter and Conte, 2009).…”

“…A limited range of activities and current coupled with pelagic eggs of C. nasus could be responsible for the frequent gene flow among populations in the middle reaches of the Yangtze River (Yuan et al, 1976;Ni et al, 1990;Xu et al, 2020). The similar results with no significant IBD pattern was also detected among populations from the lower reaches of the Yangtze and the coast of China group (R 2 = 0.056, P = 0.123), which might be derived from integrations of the upstream spawning migration behavior of anadromous individuals and transportation of juveniles by China Coastal Current (Figure 5D; Yuan et al, 1976;Yuan et al, 1980;Liu et al, 2007;Cheng, 2011;Xu et al, 2020). The Hongze Lake and Zhoukou populations belonged to the Huai River system which was connected by the Yangtze River via a human-made channel.…”

“…Compared to anadromous form, freshwater form was characterized by earlier age at maturity, shorter maxilla, smaller egg size, lower level of growth rate and smaller body size (Yuan et al, 1976;Ni et al, 1990). Although the anadromous and freshwater forms used to be regarded as different species according to their morphological and ecological differences (Yuan et al, 1976;Cheng, 2011), recent studies demonstrated that the genetic differentiation between the two forms was below the species level (Tang et al, 2007;Yang et al, 2010b;Xu et al, 2020). Until now, enough information about the phylogeographic pattern and historical demography among the freshwater and anadromous populations is missing in the Yangtze River.…”

Genomic Architecture of Rapid Parallel Adaptation to Fresh Water in a Wild Fish

“…The published chromosome-level genome assembly for C. nasus ( Xu et al. 2020 ) contains a total of 81,894 Eco RI restriction sites (one per 10 kb) across 24 linkage groups (chromosomes).…”