Combining population genomics with demographic analyses highlights habitat patchiness and larval dispersal as determinants of connectivity in coastal fish species

Abstract

Gene flow shapes spatial genetic structure and the potential for local adaptation.Among marine animals with nonmigratory adults, the presence or absence of a pelagic larval stage is thought to be a key determinant in shaping gene flow and the genetic structure of populations. In addition, the spatial distribution of suitable habitats is expected to influence the distribution of biological populations and their connectivity patterns. We used whole genome sequencing to study demographic history and reduced representation (double-digest restriction associated DNA) sequencing data to analyse spatial genetic structure in broadnosed pipefish (Syngnathus typhle).Its main habitat is eelgrass beds, which are patchily distributed along the study area in southern Norway. Demographic connectivity among populations was inferred from long-term (~30-year) population counts that uncovered a rapid decline in spatial correlations in abundance with distance as short as ~2 km. These findings were contrasted with data for two other fish species that have a pelagic larval stage (corkwing wrasse, Symphodus melops; black goby, Gobius niger). For these latter species, we found wider spatial scales of connectivity and weaker genetic isolation-by-distance patterns, except where both species experienced a strong barrier to gene flow, seemingly due to lack of suitable habitat. Our findings verify expectations that a fragmented habitat and absence of a pelagic larval stage promote genetic structure, while presence of a pelagic larvae stage increases demographic connectivity and gene flow, except perhaps over extensive habitat gaps.

Finding coarse and fine scale population structure in a coastal species: population demographics meets genomics

“…The structuring effect of this oceanographic feature in species with early life stages is also corroborated when comparing with species without such stages. A recent study showed that for the broadnosed pipefish ( Syngnathus typhle ), which gives birth to live young, this barrier effect is less pronounced, and that genetic divergence is likely due to habitat effect and isolation by distance (Knutsen et al, 2022).…”

Whole genome sequencing reveals fine-scale climate associated adaptive divergence near the range limits of a temperate reef fish

“…Genetic structuring of marine populations and adaptive differentiation has been shown to evolve despite high dispersal potential as a result of the interplay of environment, life history, and other factors influencing survival. Many marine taxa have life histories that feature pelagic egg and/or larval stages, enabling current-mediated dispersal across large distances which is thought to contribute to the low levels of genetic structuring often observed in marine fish (Levin 1996; Waples 1998; Juanes 2007; Knutsen et al . 2022).…”

“…2022), and whole genome resequencing approaches (Han et al . 2020; Knutsen et al . 2022) have with increasing levels of detail revealed significant climate or environmental associations that localize to discrete genomic regions.…”

“…For example, recent work combining pooled whole genome sequencing and double-digest sequencing methods, characterized the spatial genetic structure of broad-nosed pipefish ( Syngnathus typhle ). Additionally, comparison to other species with different life-history characteristics demonstrated the roles of fragmented habitat and an absence of a pelagic larval stage in promoting genetic structure (Knutsen et al . 2022).…”

“…Population genomics-based examinations of diversity in marine species are revealing the geographic and genomic distribution of differentiation and potential adaptive diversity. Studies using large SNP panels (Sylvester et al 2018;Watson et al 2021), reduced representation sequencing (Pratt et al 2022;Sønstebø et al 2022), and whole genome resequencing approaches (Han et al 2020;Knutsen et al 2022) have with increasing levels of detail revealed significant climate or environmental associations that localize to discrete genomic regions. For example, recent work combining pooled whole genome sequencing and double-digest sequencing methods, characterized the spatial genetic structure of broadnosed pipefish (Syngnathus typhle).…”