Population genetic structure of two congeneric deep-sea amphipod species from geographically isolated hadal trenches in the Pacific Ocean

Highlights

• In Paralicella spp. hadal trenches are not evolutionary independent units.

• Patterns of connectivity between trenches differs between species.

• RFLP species 1 has high connectivity with a small isolation-by-distance effect.

• RFLP species 2 has less connectivity with barriers to gene flow.

• Connectivity explained by trench geological ages, deep currents and seabed topography.

Abstract

The deep ocean trenches that comprise the hadal zone have traditionally been perceived as a series of geographically isolated and demographically independent features likely to promote local species endemism through potent natural selection and restricted dispersal. Here we provide the first descriptions of intraspecific population genetic structure among trenches from which the levels of genetic connectivity can be examined explicitly. A total of 109 individuals across two species of Paralicella amphipods (Lysianassoidea: Alicellidae) were genotyped at 16 microsatellite DNA loci. An analysis of molecular variance identified that 22% of the overall genetic variance was attributable to differences between the species and a further 7% was attributable to differences between populations. The two species showed different patterns of genetic structure, with the levels of genetic differentiation between trenches explained by geographical proximity, the geological ages of the trenches, contemporary bottom current patterns and seabed topography around the Pacific Ocean. Overall, the inferred levels of gene flow among trenches was sufficient to reject the hypothesis that they are evolutionarily independent units.

Introduction

The hadal zone is the deepest marine biome, extending from 6000 m to full ocean depth at approximately 11,000 m at the Challenger Deep in the Mariana Trench. It is primarily comprised of 37 trench systems which are formed along subduction zones between tectonic plates, with the majority are located around the Pacific Rim (Jamieson et al., 2010). Trenches break the continuum of the abyssal plains by forming disjunct clusters of ultra-deep habitat “islands”. The hadal zone accounts for over 45% of the total vertical depth of the marine environment (Jamieson, 2015) and it is characterised by high hydrostatic pressure, cold temperatures, low food availability and an absence of natural light (Wolff, 1960). Despite being considered an “extreme” environment the hadal zone is host to a diverse range of flora and fauna, notably the Isopoda, Polychaeta, Gastropoda and Amphipoda (Wolff, 1970, Beliaev, 1989).

The restricted distribution of key taxa within these groups to specific trenches underpins the conventional view that hadal trenches are hotspots of species endemism driven by a combination of geographic isolation and potent selection pressures (Wolff, 1960; Wolff, 1970). For example, within the amphipod genus Hirondellea, H. dubia is restricted to the Kermadec, Tonga and New Hebrides trenches in the southwest Pacific (Lacey et al., 2016), H. gigas is located in trenches in the northwest Pacific trenches studied thus far (France, 1993), and newly described Hirondellea species have been identified in the Peru-Chile Trench in the southeast Pacific (Fujii et al., 2013, Kilgallen, 2015). However, this assertion that hadal trenches are hotspots of species endemism is difficult to reconcile with the seemingly cosmopolitan distribution of other amphipod species. Chiefly, Eurythenes gryllus which has been described as having a pan-oceanic distribution from bathyal to hadal depths, and has been located in every hadal trench investigated to date in addition to the intervening abyssal plains (Barnard, 1961, Thurston et al., 2002, Havermans et al., 2013, Eustace et al., 2016). This cosmopolitan distribution of a supposedly single E. gryllus species is complicated by morphological and phylogeographic differences between different global populations (Havermans et al., 2013) and even within a single trench population (Eustace et al., 2016). This suggests E. gryllus actually represents multiple species each defined by geographic and bathymetric isolation and associated drift and selection (Havermans, 2016).

A capacity for hadal trenches to promote genetic divergence within and between species appears counter to the depth-differentiation hypothesis (Rex and Etter, 2010). This states there should be a reduction in barriers to gene flow with increasing depth from the continental shelf due to the increase in environmental homogeneity with bathymetric depth. A growing body of data from across deep-sea environments in the bathyal and abyssal zones supports the depth-differentiation hypothesis, largely showing connectivity between populations (e.g. Cowart et al., 2014; Quattrini et al., 2015; Ritchie et al., 2013). It is unclear how disjunct topographical features such as seamounts, spreading centres (ridges), fracture zones and canyons disrupt the depth differentiation paradigm, but it appears patterns of genetic structure are variable across taxa, life history strategies and geographic locations (Baco et al., 2016, Clark et al., 2010). To date there has been no indication of how the hadal zone fits into the depth-differentiation hypothesis paradigm. Primarily because of the dearth of information on population genetic structure based upon the distribution of neutral genetic variation. A demonstration that hadal trenches have equivalent frequencies of neutral polymorphisms would indicate a high degree of connectivity, and conversely significant genetic structure would highlight that each trench represents a demographically independent unit with minimal gene flow. Examining the patterns of gene flow in the context of trench location, geological ages of trenches, topographical features of the abyssal plains and contemporary bottom currents will allow speculation on possible routes of historical colonisation of the hadal trenches and identify the major drivers influencing patterns of dispersal at an oceanic scale.

Here we examine the patterns of genetic structure between populations of two Lysianassoid amphipods, Paralicella tenuipes and P. caperesca, across five trenches around the Pacific Rim. The two sister species from the Paralicella genus provide an excellent model for testing patterns of gene flow as they are characteristic of the abyssal fauna with an abyssal-hadal distribution (Barnard and Schulenberger, 1969; De Broyer et al., 2004) allowing us to examine differences between trenches in the context of dispersal patterns across the intervening abyssal plains. P. tenuipes and P. caperesca also have overlapping pan-oceanic geographical distributions (Barnard and Shulenberger, 1969; Thurston, 1979) that will facilitate examination of parallel patterns of connectivity across trench populations across the species.

This study represents the first investigation elucidating patterns of gene flow and connectivity between hadal trenches. We exploit a suite of microsatellite DNA markers that were previously mined from an Illumina MiSeq library of P. tenuipes (Ritchie et al., 2016) to test the null hypothesis that there is extensive gene flow between trench populations, in both species, leading to a lack of significant population genetic structure.