Post‐glacial establishment of locally adapted fish populations over a steep salinity gradient

Abstract

Studies of colonization of new habitats that appear from rapidly changing environments are interesting and highly relevant to our understanding of divergence and speciation. Here, we analyse phenotypic and genetic variation involved in the successful establishment of a marine fish (sand goby, Pomatoschistus minutus) over a steep salinity drop from 35 PSU in the North Sea (NE Atlantic) to two PSU in the inner parts of the post-glacial Baltic Sea. We first show that populations are adapted to local salinity in a key reproductive trait, the proportion of motile sperm. Thereafter, we show that genome variation at 22,190 single nucleotide polymorphisms (SNPs) shows strong differentiation among populations along the gradient. Sequences containing outlier SNPs and transcriptome sequences, mapped to a draft genome, reveal associations with genes with relevant functions for adaptation in this environment but without overall evidence of functional enrichment. The many contigs involved suggest polygenic differentiation. We trace the origin of this differentiation using demographic modelling and find the most likely scenario is that at least part of the genetic differentiation is older than the Baltic Sea and is a result of isolation of two lineages prior to the current contact over the North Sea-Baltic Sea transition zone.

Whole-genome sequencing reveals sex determination and liver high-fat storage mechanisms of yellowstripe goby (Mugilogobius chulae)

“…Unfortunately, neither the genome sequence and phylogenetic relationships of many groups of gobies nor the laboratory breeding and rearing methods are resolved. Only a few gobiid genomes have been sequenced, such as those of round goby (Neogobius melanostomus) 8 , mudskippers (Boleophthalmus pectinirostris, Periophthalmodon schlosseri, Periophthalmus magnuspinnatus, Scartelaos histophorus) 10 , and sand goby (Pomatoschistus minutus) 29 . Currently, only a few small fish species [e.g., zebrafish 30 , Japanese medaka (Oryzias latipes) 31 , and platyfish (Xiphophorus maculatus) 32 ] have been widely used in the laboratory; however, the large majority of these inhabit freshwater environments.…”

Pipefish Locally Adapted to Low Salinity in the Baltic Sea Retain Phenotypic Plasticity to Cope With Ancestral Salinity Levels

“…The brackish salinity environment in the Baltic Sea imposes osmoregulatory stress on marine animals and is thus assumed to be an important driver for genetic divergence and adaptation to local condition (Berg et al, 2015;Guo et al, 2015;Johannesson et al, 2020). Strong genetic clines over the Baltic Sea salinity gradient were shown for a diversity of species (Johannesson et al, 2020) with strong patterns of local salinity adaptation (Leder et al, 2021). Here, we focused on six pipefish populations from the German coastline A PERMANOVA was applied to gene expression (− Ct values) of all 558 samples for all genes (47), including immune genes comprised of the innate, adaptive and complement genes, as well as genes involved in metabolism, osmoregulation and epigenetics, e.g., methylation or histone modification.…”

Speciation in marine environments: Diving under the surface

“…In this issue, Leder et al. (2021) used such a data set to infer the historical demography associated with speciation in sand gobies that inhabit a steep salinity gradient between the Baltic Sea and the North Sea. Many of the successful colonizers of the Baltic Sea show evidence of adaptation to lower salinity and reproductive isolation from North Sea populations (Johannesson et al., 2020).…”

“…Johannesson et al., 2020; Westram et al., 2018) (also, see Section 2.5 ) . Although not very frequent, detailed studies of hybrid zones in marine environments have provided important information about the role of local adaptation in speciation (Kess et al., 2021; Leder et al., 2021; Prada & Hellberg, 2021; Westram et al., 2018), the presence of genetic incompatibilities (Simon et al., 2021) or the coupling between these two types of barriers (Bierne, 2011). Extensive mixing in hybrid zones may also make it possible to identify candidate SNPs or genomic regions underlying reproductive barriers through genome‐wide association tests (Duranton et al., 2020).…”

“…As Leder et al. (2021) point out, distinguishing alternative demographic histories is difficult even with modern genomic data sets, so individual studies should be interpreted with some caution (see also Momigliano et al., 2020). However, by applying a similar approach to many marine organisms inhabiting a broad range of environments, we may eventually be able to address more general questions about the history of speciation in our oceans.…”