Genomics of habitat choice and adaptive evolution in a deep-sea fish

Abstract

W hile longitudinal and latitudinal habitat transitions have been proposed to define marine communities and promote intraspecific differentiation 1-3 , little is known about the importance of transitions along ocean depth gradients 4,5 , although substantial changes in species assemblages with depth have been recorded (for example, ref. 6 ), and relatively narrow depth ranges may distinguish closely related species (for example, refs 7,8 ). Understanding the relevant mechanisms will contribute significantly to our understanding of eco-evolutionary processes and the origin of marine biodiversity. We chose the roundnose grenadier (Coryphaenoides rupestris) as a model system because it is a widespread species that can inhabit a comparatively broad range of depths 9 from ~180 m to 2,600 m. It is a batch spawner, producing up to 69,000 pelagic eggs per female 10 . It has a spawning season peaking in autumn 11 (recent observations were in September at 1,500 m; ref. 12 ), preys on fish, cephalopods and invertebrates in both benthic and pelagic habitats 13 , and shows minor genetic differentiation across its geographic range [14][15][16] .Adaptation to habitat can occur among populations within a species, and if disruptive selection is associated with assortative mating has the potential to promote incipient speciation through ecological processes in sympatry 17 . When environmental change exposes new habitats and niche potential, adaptive radiations may rapidly generate a new lineage of species 18,19 . To the extent that differential selection can retain polymorphisms within or among populations, this may facilitate the process of adaptive radiation. Here, we focus on one of the key habitat transitions in the oceans-between the photic mesopelagic region and the aphotic regions below (together with the more contiguous changes associated with increasing depth). There is the potential for species (such as the roundnose grenadier), whose habitat range extends across this boundary or along the depth gradient, to experience differential selective pressures. We tested hypotheses about adaptation to these deep-sea habitats using genome sequence data together with data on the ecology and life history of the subject species. We found that juvenile fish of this species are found primarily in relatively shallow depths (near the transition between the mesopelagic and bathypelagic zones) and then migrate as they mature to different depths, and this is strongly associated with their genotype at a set of functional loci. In particular, all adults below ~1,800 m share the same homozygous genotype at each locus. There is evidence for strong selection maintaining this difference, but no clear evidence for differentiation driven by assortative mating. Results and discussionWe produced an annotated reference genome for C. rupestris with a total length of 0.829 gigabase pairs, a mean depth of 104× and an N50 of 159,738 (see Supplementary Methods for details). We used this draft genome to map 60 additional genomes sequenced to a mean depth ...

Genomic data suggest environmental drivers of fish population structure in the deep sea: A case study for the orange roughy (Hoplostethus atlanticus)

“…Our data reflecting local adaptation in adults may therefore represent populations of individuals that had a broader or distinct distribution at earlier life‐history stages. An interesting parallel example may be the depth distribution of the roundnose grenadier ( Coryphaenoides rupestris ) in the eastern NA, where sympatric juveniles of distinct genotypes at specific functional loci (with fixed non‐synonymous variants) segregate to different depths as adults depending on their genotype (Gaither et al, ). Carlsson et al () also suggest subtle genetic differentiation ( F ST = 0.004–0.01) from the Porcupine Bank area comparing samples from ‘flat’ and ‘mound’ habitats during spawning periods based on eight microsatellite DNA loci.…”

“…This would involve the consideration of stock designations for the preservation of local adaptive characteristics independent of the level of movement, since selection can maintain the difference despite ongoing gene flow through dispersal (e.g. Gaither et al, ).…”

Deep‐water fisheries along the British Isles continental slopes: status, ecosystem effects and future perspectives

“…Geochemical analysis of C. rupestris otoliths showed a clear separation of population units along the NE Atlantic Ocean (Longmore et al , , ). A complex depth‐dependent genetic structure in C. rupestris was revealed recently (Gaither et al , ) identifying genetically based ontogenetic depth segregation whereby juvenile populations inhabiting shallow waters exhibit mixing, but adults segregate by depth forming genetically distinct populations. In contrast, the roughhead grenadier Macrourus berglax Lacépède 1801 shows significant gene flow across North Atlantic locations (Coscia et al , ).…”

Shared genomic outliers across two divergent population clusters of a highly threatened seagrass

“…Although neutral variation can reveal much about a species demographic history, in many cases, patterns revealed from outlier loci can provide unique insights into evolutionary potential and patterns of resilience (Stapley et al 2010;Guo et al 2015;Funk et al 2016;Gaither et al 2018). Particularly in marine systems where gene flow is generally presumed to be high, signals of outlier loci can help detect population structure (André et al 2011;Freamo et al 2011;Hess et al 2013;Candy et al 2015;Araneda et al 2016;Tigano & Friesen 2016;Attard et al 2018).…”