The origins of limnetic forms and cryptic divergence in Gnathopogon fishes (Cyprinidae) in Japan

The cyprinid species of the genus Gnathopogon, exhibiting flexible morphological and ecological variation, include limnetic life forms. We examined the origin of the limnetic forms and the population divergence of the Japanese Gnathopogon species, using molecular phylogenetic and phylogeographic analyses. A Bayesian phylogenetic inference approach based on mtDNA cytochrome b sequence data revealed three major lineages in G. elongatus. One of them formed a monophyletic group with the limnetic species G. caerulescens, which is endemic to an ancient lake, Lake Biwa. The divergence of the G. caerulescens lineage was estimated to date back to the early Pleistocene. This precedes the formation of the extensive pelagic environment in the present Lake Biwa. However, the recent genetic divergence of G. caerulescens was inferred to originate in the present Lake Biwa in the late Pleistocene. Another lacustrine population in the Mikata Lakes was shown to belong to a different lineage from G. caerulescens. The majority of the population possessed unique, but non-monophyletic, haplotypes, suggesting a short evolutionary history. One of the cryptic lineages of G. elongatus discovered in the Ina Valley, the lower area of Lake Suwa, might be related to the extinct lacustrine subspecies G. elongatus suwae, which has been replaced by introduced congeners. The previous and ongoing introductions of Gnathopogon fishes would have produced genetic disturbance to the indigenous populations

Data from: Molecular signatures of lineage-specific adaptive evolution in a unique sea basin: the example of an anadromous goby Leucopsarion petersii

Climate changes on various time scales often shape genetic novelty and adaptive variation in many biotas. We explored molecular signatures of directional selection in populations of the ice goby Leucopsarion petersii inhabiting a unique sea basin, the Sea of Japan, where a wide variety of environments existed in the Pleistocene in relation to shifts in sea level by repeated glaciations. This species consisted of two historically allopatric lineages, the Japan Sea (JS) and Pacific Ocean (PO) lineages, and these have lived under contrasting marine environments that are expected to have imposed different selection regimes caused by past climatic and current oceanographic factors. We applied a limited genome-scan approach using seven candidate genes for phenotypic differences between two lineages in combination with 100 anonymous microsatellite loci. Neuropeptide Y (NPY) gene, which is an important regulator of food intake and potent orexigenic agent, and three anonymous microsatellites were identified as robust outliers, that is, candidate loci potentially under directional selection, by multiple divergence- and diversity-based outlier tests in comparisons focused on multiple populations of the JS vs. PO lineages. For these outlier loci, populations of the JS lineage had putative signals of selective sweeps. Additionally, real-time quantitative PCR analysis using fish reared in a common environment showed a higher expression level for NPY gene in the JS lineage. Thus, this study succeeded in identifying candidate genomic regions under selection across populations of the JS lineage and provided evidence for lineage-specific adaptive evolution in this unique sea basin

Kokita et al 2013 MEC

Genotyping data of anonymous microsatellite and candidate gene markers (107 loci). The data set consists of samples from four populations (AM, FK, SZ and WK). See Kokita et al. (2013) for further details. The data file is in MSA format [Dieringer D, Schlotterer C (2003) Microsatellite Analyser (msa): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes, 3, 167–169]

Centroid sizes of the samples from natural populations

Centroid sizes of the samples from the natural populations in NTS format. The numbers and the population codes (see supplementary Table S1) of the analysed populations are: 11 E1T, 20 E1S, 34 E1D, 32 E1M, 8 E2H, 18 E2R, 10 E2K, 6 E2I, 14 E3K, 10 E3I, 3 S, 28 CM, and 12 CN, in this order

Data from: Genomic architecture of habitat-related divergence and signature of directional selection in the body shapes of Gnathopogon fishes

Evolution of ecomorphologically relevant traits such as body shapes is important to colonize and persist in a novel environment. Habitat-related adaptive divergence of these traits is therefore common among animals. We studied the genomic architecture of habitat-related divergence in the body shape of Gnathopogon fishes, a novel example of lake–stream ecomorphological divergence, and tested for the action of directional selection on body shape differentiation. Compared to stream-dwelling Gnathopogon elongatus, the sister species Gnathopogon caerulescens, exclusively inhabiting a large ancient lake, had an elongated body, increased proportion of the caudal region and small head, which would be advantageous in the limnetic environment. Using an F2 interspecific cross between the two Gnathopogon species (195 individuals), quantitative trait locus (QTL) analysis with geometric morphometric quantification of body shape and restriction-site associated DNA sequencing-derived markers (1622 loci) identified 26 significant QTLs associated with the interspecific differences of body shape-related traits. These QTLs had small to moderate effects, supporting polygenic inheritance of the body shape-related traits. Each QTL was mostly located on different genomic regions, while colocalized QTLs were detected for some ecomorphologically relevant traits that are proxy of body and caudal peduncle depths, suggesting different degree of modularity among traits. The directions of the body shape QTLs were mostly consistent with the interspecific difference, and QTL sign test suggested a genetic signature of directional selection in the body shape divergence. Thus, we successfully elucidated the genomic architecture underlying the adaptive changes of the quantitative and complex morphological trait in a novel system

A RAD-based linkage map and comparative genomics in the gudgeons (genus <it>Gnathopogon</it>, Cyprinidae)

<p>Abstract</p> <p>Background</p> <p>The construction of linkage maps is a first step in exploring the genetic basis for adaptive phenotypic divergence in closely related species by quantitative trait locus (QTL) analysis. Linkage maps are also useful for comparative genomics in non-model organisms. Advances in genomics technologies make it more feasible than ever to study the genetics of adaptation in natural populations. Restriction-site associated DNA (RAD) sequencing in next-generation sequencers facilitates the development of many genetic markers and genotyping. We aimed to construct a linkage map of the gudgeons of the genus <it>Gnathopogon</it> (Cyprinidae) for comparative genomics with the zebrafish <it>Danio rerio</it> (a member of the same family as gudgeons) and for the future QTL analysis of the genetic architecture underlying adaptive phenotypic evolution of <it>Gnathopogon</it>.</p> <p>Results</p> <p>We constructed the first genetic linkage map of <it>Gnathopogon</it> using a 198 F₂ interspecific cross between two closely related species in Japan: river-dwelling <it>Gnathopogon elongatus</it> and lake-dwelling <it>Gnathopogon caerulescens</it>. Based on 1,622 RAD-tag markers, a linkage map spanning 1,390.9 cM with 25 linkage groups and an average marker interval of 0.87 cM was constructed. We also identified a region involving female-specific transmission ratio distortion (TRD). Synteny and collinearity were extensively conserved between <it>Gnathopogon</it> and zebrafish.</p> <p>Conclusions</p> <p>The dense SNP-based linkage map presented here provides a basis for future QTL analysis. It will also be useful for transferring genomic information from a “traditional” model fish species, zebrafish, to screen candidate genes underlying ecologically important traits of the gudgeons.</p

Plate reduction in southern Japanese freshwater populations of threespine stickleback (Gasterosteus aculeatus)

Abstract Adaptation to similar environments can lead to the evolution of similar phenotypes in phylogenetically independent lineages. However, the extent of parallel evolution often varies. Because such variations can be due to environmental heterogeneity among seemingly similar habitats, identification of the environmental factors that cause non‐parallel patterns can provide valuable insight into the ecological factors associated with phenotypic diversification. Armor plate reduction in replicate freshwater populations of the threespine stickleback (Gasterosteus aculeatus) represents a well‐known example of parallel evolution. Many freshwater populations in multiple regions of the Northern Hemisphere have reduced plate numbers, but not all freshwater populations exhibit plate reduction. In this study, we characterized plate number variation in Japanese freshwater populations and investigated the association between plate number and several abiotic environmental factors. We found that most freshwater populations have not reduced plate numbers in Japan. Plate reduction tends to occur in habitats with warmer winter temperatures at lower latitudes in Japan. In contrast, low dissolved calcium levels or water turbidity had no significant effects on plate reduction, although these were reported to be associated with plate reduction in Europe. Although our data are consistent with the hypothesis that winter temperatures are associated with plate reduction, further studies on the relationship between temperatures and fitness using sticklebacks with varying plate numbers are necessary to confirm this hypothesis and understand the factors causing variations in the extent of parallel evolution

Accumulation of Deleterious Mutations in Landlocked Threespine Stickleback Populations

Abstract Colonization of new habitats often reduces population sizes and may result in the accumulation of deleterious mutations by genetic drift. Compared with the genomic basis for adaptation to new environments, genome-wide analysis of deleterious mutations in isolated populations remains limited. In the present study, we investigated the accumulation of deleterious mutations in five endangered freshwater populations of threespine stickleback (Gasterosteus aculeatus) in the central part of the mainland of Japan. Using whole-genome resequencing data, we first conducted phylogenomic analysis and confirmed at least two independent freshwater colonization events in the central mainland from ancestral marine ecotypes. Next, analyses of single nucleotide polymorphisms showed a substantial reduction of heterozygosity in freshwater populations compared with marine populations. Reduction in heterozygosity was more apparent at the center of each chromosome than the peripheries and on X chromosomes compared with autosomes. Third, bioinformatic analysis of deleterious mutations showed increased accumulation of putatively deleterious mutations in the landlocked freshwater populations compared with marine populations. For the majority of populations examined, the frequencies of putatively deleterious mutations were higher on X chromosomes than on autosomes. The interpopulation comparison indicated that the majority of putatively deleterious mutations may have accumulated independently. Thus, whole-genome resequencing of endangered populations can help to estimate the accumulation of deleterious mutations and inform us of which populations are the most severely endangered. Furthermore, analysis of variation among chromosomes can give insights into whether any particular chromosomes are likely to accumulate deleterious mutations