Adaptation and drift in the deep sea - investigating the evolution of diversity in a 'uniform' environment

The conservation of biodiversity is necessary to provide natural populations with the potential to respond to a changing environment, and to prevent the loss of fitness associated with lost diversity. An understanding the underlying processes is necessary to promote effective transferable management strategies. This is especially important in the marine environment where there are few obvious boundaries to gene flow. Biodiversity is lost within populations by drift & directional selection, and retained among populations by the same processes. The size of insular populations helps to determine the dominant process, since drift is stronger than selection in small populations. It is known that much natural diversity is divided among conspecific populations by these processes, but the fragmented structure of this diversity is often cryptic, especially in poorly understood environments like the deep sea.

We typically define populations a priori by geographic distance and according to apparent physical boundaries. However, in addition to spatial factors, environmental characteristics can affect patterns of connectivity by affecting the rate and direction of gene flow, and this influence will vary as environments change over time. Environmental characteristics also drive local selection, and selection can maintain differences among populations even with continuing gene flow. Without knowledge about how local populations may have adapted to local environments, we remain unable to incorporate that type of biodiversity into conservation strategy, and to address its potential importance to the long-term survival of species. Understanding the function and value of biodiversity requires a better understanding of the interacting processes of selection and drift leading to its evolution and loss. While much of the relevant theory is well established, empirical data are required to test theory and determine how environmental factors interact with evolutionary processes in natural systems.

In this study we will employ second generation sequencing technologies to investigate how environmental factors are associated with the evolution of population structure and speciation in the deep sea, at both neutral and functional loci. The particular focus will be on habitat depth and isolation by distance, however other environmental factors will be quantified at collection sites based on data collected from the same sites during the recent ECOMAR consortium study (during which samples for the proposed study were collected). The study species will be fish in the genus Coryphaenoides, a specious genus of deep demersal fishes, some of which are commercially important fisheries species (including the primary focal species in this study, C. rupestris). Initial studies have shown phylogenetic lineage division correleted to habitat depth. Other work has indicated selection at genes associated with adaptation to pressure in some of these species. Two focal Coryphaenoides species will be investigated in a comparative population genomics study. These species, C. rupestris and C. brevibarbis are sympatric, but the former is found at shallower depths than the latter. We will test hypotheses about how habitat division by depth or other characteristics (e.g. current systems or geographic distance) may determine the evolution of intra- and inter-specific diversity (including among multiple habitat-specialist species in the genus using an extended phylogenetic assessment) both by drift (through differential environmental pressures associated with dispersal) and by selection. Greater connectivity is predicted in the abyssal habitat, which may lead to larger effective population sizes and facilitate adaptive evolution. Taken together these data will provide novel insight into the interactive role of drift and selection during the evolution of diversity, and transferable inference about how diversity is structured in the deep sea.

The primary impact of this work beyond the beneficiaries in the academic community will be on fisheries management and commercial fisheries working in the deep sea. In the eastern North Atlantic (including the high seas area out to and including the mid-Atlantic ridge) deep-sea fisheries management comes under the jurisdiction of the European Commission and the North-East Fisheries Commission (NEAFC). Deep-sea stocks are defined as those living at depths of 400m or greater. Although fishing by factory trawlers and modern longliners started in the eastern North Atlantic in the late 1960s, regulation was introduced only recently, beginning in 2002 with the introduction of the first 'total allowable catch' (TAC) quotas (setting quotas for 2003). This covered eight species, among which was the roundnose grenadier (Coryphaenoides rupestris, a focal subject species in this study). Two further species were later added together with a quota for a collection of 11 deep-sea shark species (considered together) for 2005 and 2006. TAC allowances are now set for a given EC country and ICES fisheries region separately. One recognised problem with this approach is that deep-sea fisheries are typically multi-species in character, based on trawling or gil-net fisheries. A targeted species allowance assumes that there is a simple relationship between the recorded landing records and effort for that species, which is unlikely to be the case in multi-species fisheries. This could mean that there is greater impact from fisheries for a given species than indicated in the catch records, and so greater impact on genetic diversity. In 2009 the NEAFC agreed to adopt a measure that closed 330,000 square km to bottom fishing at the mid-Atlantic ridge, including our core study area in that region near the Charlie Gibbs Fracture Zone. There are concerns about the effectiveness of this measure as well, as many of the target species have different geographic distributions at different life stages, likely including the grenadier species in this study, due to larval drift on oceanic currents (and regions near the study area at the mid-Atlantic ridge remain a focus of roundnose grenadier fisheries).

Our data will help to resolve this question. The roundnose grenadier has had the highest quota assigned among all of the managed species, with a total of 12,443 tonnes allowed in 2005 falling to 8,109 tonnes for 2011 (but still the highest TAC quota for a deep-sea fish). However, little is know for any of the subject species about whether or not regional populations should be managed separately. Our study will address this question for the roundnose grenadier for most regions of primary importance to the fishery (ICES areas VI, VII & XII) using a very high resolution methodology, however of greater importance will be the general assessment of drivers of stock structuring in the deep sea, and insight into the best methods for assigning management areas. We will also provide detailed information on the distribution of diversity at functional genetic markers for the first time for a deep sea fish species, and assess their potential relevance in biodiversity conservation and management. Details of our findings will be brought to the attention of the NEAFC and European Commission for consideration. Deep-sea fisheries managers will be among those included in our program of end-user engagement. Other interested end users will include the general public with an interest in life in the deep sea. Through recent involvement in the Census of Marine Life project MARECO (focussed on life in the deep sea at the mid-Atlantic ridge), it was evident that our outreach for that project was highly popular and successful, indicating a broad interest in discoveries about this largely unknown ecosystem. We will establish a web page providing explanations for a lay audience, updates, images and news and also publish in the popular media.