Adapting to habitat depth in the deep sea

Like Comment

The paper in Nature Ecology & Evolution is here:

The roundnose grenadier (Coryphaenoides rupestris) lives over a surprisingly broad range of habitat depths (~260-2600m), with a distribution range extending across the North Atlantic.  We began studying this species in association with the Census of Marine Life and the ‘MAR-ECO’ research program ( 15 years ago.  Our initial interest was in the potential for larval drift on oceanic currents to generate patterns of differentiation among populations of this bathypelagic fish, and we found some evidence for it either side of the sub-polar front, where current systems diverge in the North Atlantic (White et al. 2010).  Later our focus turned to the potential for diversification in this species in a vertical dimension, reflecting habitat transitions across two kilometres of ocean depth.  The first indication was based on relatively few data, showing an allele frequency association with depth at a single microsatellite DNA locus, apparently linked to a gene under selection (White et al. 2010).  This inspired the more recent study.  

We had found evidence for differentiation with depth at a location off the Hebrides, where the slope descends quickly into the Rockall Trough.  We returned there to collect fish from specific depths along a gradient, descending from 750m to 1800m down the slope.  This transect crosses an important transitional zone in the oceans, from the relatively vibrant mesopelagic, fuelled by sunlight and phytoplankton, down into the bathypelagic, devoid of light.  This time our objective was to search the genome for further evidence of adaptation associated with depth, driven by natural selection.  We generated an annotated reference genome for the species so that we could consider gene function for any divergent loci.  We then re-sequenced 60 genomes from adult fish along the depth gradient (Gaither et al. 2018).  The samples had all been collected during the same day within 25km of each other, and so confounding horizontal spatial or temporal differentiation was unlikely.  

Comparing genomes along the transect revealed multiple genotypes strongly correlated with depth, and among them 9 non-synonymous changes in six coding genes.  These were fixed homozygous for a particular allele at each locus at 1800m, and dominated by a different allele at shallower depths.  There was furthermore evidence for strong disruptive selection and both differentiation by depth and disruptive selection across the species range for these loci.  Gene ontology analyses suggested functions mostly associated with development and morphogenesis.  At the same time, neutral loci showed no pattern of differentiation associated with depth, and so no clear signal for assortative mating.  

In this species it appears that juveniles are only found at approximately 1000m, and then remain there or migrate to greater depths as they mature.  The genotypes of sampled juveniles were mixed, indicating that they later segregate to different depths according to their genotypes (since adults are segregated by genotype).  So the inference is for continuing selection for different ecotypes adapted to life either side of the mesopelagic, bathypelagic boundary in a fish whose habitat extends well beyond that boundary in both directions.  At the same time there was no strong evidence for insipient speciation between these ecotypes, but rather a continuing pressure in support of local adaptation.

This provides a uniquely clear example of how different specialisations ('ecotypes'), in this case adapted to life at different habitat depths, can be maintained within the same species, even without segregation among different geographic populations. This might help prepare a species for a rapid response to a changing environment while partitioning resources among individuals best prepared to exploit them.  In this case differentiation among ecotypes may be driven by the distinction between a resource rich environment within the mesopelagic, and a relatively resource poor environment deeper down the slope.

Gaither, M.R., Gkafas, G.A., de Jong. M., Sarigol, F., Neat, F., Regnier, T., Moore, D., Grӧcke, D.R., Hall, N., Liu, X., Kenny, J., Lucaci, A., Hughes, M., Haldenby, S., Hoelzel, A.R. (2018) Genomics of habitat choice and adaptive evolution in the deep sea.  Nature Ecology & Evolution 10.1038/s41559-018-0482-x

White, T.A., Stamford, J. & Hoelzel, A.R. 2010. Local selection and population structure in a deep-sea fish, the roundnose grenadier (Coryphaenoides rupestris). Mol. Ecol. 19:216-226.

A. Rus Hoelzel

Professor, Durham University

Evolutionary Biology