Invertebrate population genetics across Earth's largest habitat: The deep‐sea floor

Abstract

Despite the deep sea being the largest habitat on Earth, there are just 77 population genetic studies of invertebrates (115 species) inhabiting non-chemosynthetic ecosystems on the deep-sea floor (below 200 m depth). We review and synthesize the results of these papers. Studies reveal levels of genetic diversity comparable to shallow-water species. Generally, populations at similar depths were well connected over 100s-1,000s km, but studies that sampled across depth ranges reveal population structure at much smaller scales (100s-1,000s m) consistent with isolation by adaptation across environmental gradients, or the existence of physical barriers to connectivity with depth. Few studies were ocean-wide (under 4%), and 48% were Atlanticfocused. There is strong emphasis on megafauna and commercial species with research into meiofauna, "ecosystem engineers" and other ecologically important species lacking. Only nine papers account for~50% of the planet's surface (depths below 3,500 m). Just two species were studied below 5,000 m, a quarter of Earth's seafloor.Most studies used single-locus mitochondrial genes revealing a common pattern of non-neutrality, consistent with demographic instability or selective sweeps; similar to deep-sea hydrothermal vent fauna. The absence of a clear difference between vent and non-vent could signify that demographic instability is common in the deep sea, or that selective sweeps render single-locus mitochondrial studies demographically uninformative. The number of population genetics studies to date is miniscule in relation to the size of the deep sea. The paucity of studies constrains meta-analyses where broad inferences about deep-sea ecology could be made.

Implications of population connectivity studies for the design of marine protected areas in the deep sea: An example of a demosponge from the Clarion‐Clipperton Zone

“…Testing environmental factors responsible for the genetic structure observed is a major goal in ecological analysis and, at the same time, is one of the major challenges for studies aiming to describe genetic connectivity in the deep sea (Hansen & Hemmer-Hansen, 2007;Taylor & Roterman, 2017). To our knowledge, the combination of ecological and physical models and population genetics has been attempted for relatively few studies of deep sea organisms but has usually provided greater insights into the factors ultimately determining connectivity among populations (Dambach, Raupach, Leese, Schwarzer, & Engler, 2016;Jorde et al, 2015).…”

“…To achieve this, the evaluation of species' ranges and their levels of population connectivity and turnover are needed (Baco et al, 2016). Efforts to determine the population genetic connectivity in deep sea invertebrates have mainly been focused on chemosynthetic environments (Taylor & Roterman, 2017;Vrijenhoek, 2010). However, as stated by Taylor and Roterman (2017) in their recent review, the ephemeral nature and non-equilibrium conditions characteristic of these particular habitats could limit their comparability to other more common and stable deep sea habitats.…”

“…However, as stated by Taylor and Roterman (2017) in their recent review, the ephemeral nature and non-equilibrium conditions characteristic of these particular habitats could limit their comparability to other more common and stable deep sea habitats. Molecular connectivity of marine invertebrates in non-chemosynthetic deep sea habitats has barely been assessed, and two recent reviews on this topic (Baco et al, 2016;Taylor & Roterman, 2017) concluded that there is a clear need to assess the connectivity of deep sea organisms from a variety of habitats, life history types, taxonomic groups and depth zones. This is especially true for studies at abyssal depths and deeper since, to date, there is only one genetic study of species occurring below 5,000 m depth (Ritchie, Jamieson, & Piertney, 2017).…”

Shell morphology and color of the subtidal whelk Buccinum undatum exhibit fine‐scaled spatial patterns

“…Phenotypic diversity and spatial variation in gastropod shell morphology have been well studied in intertidal and limnetic systems (Bourdeau et al, 2015;Johannesson, 2015;Johannesson, Johannesson, & Butlin, 2016;Rolán-Alvarez, Austin, & Boulding, 2015;Trussell & Etter, 2001;Williams, 2017). However, there is a noticeable paucity of knowledge on geographical patterns, population connectivity, and within-species diversity in marine species (Conover, Clarke, Munch, & Wagner, 2006), particularly in deep sea (>200 m depth) habitats (Mengerink et al, 2014;Taylor & Roterman, 2017) but also in shallower, coastal seas. These coastal zones are home to many commercially harvested gastropods, for which spatial management and conservation strategies are hampered by a scarcity of data on population processes (Jones et al, 2007;Kough et al, 2017;Leis et al, 2011;Machkour-M'Rabet, Cruz-Medina, García-De León, De Jesús-Navarrete, & Hénaut, 2017;Woods & Jonasson, 2017).…”

Species-specific genetic variation in response to deep-sea environmental variation amongst Vulnerable Marine Ecosystem indicator taxa

“…Whilst there is, at present, no indication that the patterns of species-specific genetic structuring are attributable to local or regional adaptation, the recognition of its existence as a pre-existing condition for seascape genetics analyses is important. Typically, genetic differentiation is described using neutral markers 33,39 , but with new marker types and new analytical procedures there is increasing focus on non-neutral markers (genes or non-coding regions closely linked to genes), at least some of which may be of particular value in determining the cause and functional mechanism of pronounced patterns of genetic structure that may arise as a consequence of selection 15,34,37,40,41 .…”