Population genetic structure of two congeneric deep-sea amphipod species from geographically isolated hadal trenches in the Pacific Ocean
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.
Section snippets
Sample collection
A total of 109 amphipods were collected from across five hadal trenches over the course of six sampling campaigns between 2007 and 2013 using an autonomous deep-ocean lander vehicle (Jamieson et al., Jamieson et al., 2009a, Jamieson et al., 2009b, 2009b) incorporating small baited funnel traps (see Table 1 and Ritchie et al., 2015). Upon recovery of the lander, amphipods were transferred immediately to 99% ethanol prior to morphological identification to genus level in a shore-based laboratory
Results
Samples collected from the deep sea often yield poor quality DNA due to the extreme change in hydrostatic pressure which results in cell and DNA damage (Dixon et al., 2004), plus DNA degradation caused by inevitable time between collection and preservation (Hofreiter et al., 2001). This can lead to loss of individual genotypes across samples. Here we based analysis on samples that yielded over 80% amplification success, and through trial analysis using jack-knifed datasets confirmed that
Discussion
The salient finding of this study is that there is a level of genetic structure between Paralicella spp. amphipods from the different trenches but this is not at a level that would indicate that hadal trenches are demographically and evolutionary independent units. This finding is counter to the traditionally perceived view point that trenches represent geographically and genetically isolated habitats that promote high levels of species endemism. The levels of genetic structure observed are
Acknowledgements
This work was supported by the HADEEP projects, funded by the Nippon Foundation, Japan (2009765188), the Natural Environmental Research Council, UK (NE/E007171/1) and the Total Foundation, France. We acknowledge additional support from the Marine Alliance for Science and Technology for Scotland (MASTS) funded by the Scottish Funding Council (Ref: HR09011) and the Leverhulme Trust (to SBP). Additional sea time was supported by NIWA's ‘Impact of Resource Use on Vulnerable Deep-Sea Communities’
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2018, Deep-Sea Research Part II: Topical Studies in OceanographyCitation Excerpt :This method has become favourable for reasons such as financial risk to reward ratio (relatively inexpensive compared to ROV/HOV), a method relatively unaffected by depth (unlike trawling), and reasonably well-suited to the types of complex topography found in trenches. Landers have therefore led to a wave of observational studies (Hessler et al., 1978; Aguzzi et al., 2012; Jamieson et al., 2009a, 2009b, 2011a, 2011b, 2012a, 2012b, 2013), leading to ever increasingly large data sets (Linley et al., 2016, 2017), which when combined with baited traps have shown great progress in ecology (Blankenship et al., 2006; Blankenship and Levin, 2007; Fujii et al., 2013; Lacey et al., 2016), and molecular studies (Ritchie et al., 2015, 2016, 2017, this issue). Water sampling landers for microbial studies are now also common place (Eloe et al., 2011a, 2011b; Nunoura et al., 2015, 2016, Tarn et al., 2016).
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2018, Deep-Sea Research Part II: Topical Studies in OceanographyCitation Excerpt :Furthermore, the recent increases in sampling effort at hadal depths over extensive bathymetric ranges and across multiple trenches is permitting inferences to be made on community and population structure at both intra- and inter-trench levels for the first time (Fujii et al., 2013; Lacey et al., 2016). As such, hadal amphipods have been the subject of numerous and diverse studies in recent years (Blankenship et al., 2006; Blankenship and Levin, 2007; Jamieson et al., 2011a; Kobayashi et al., 2012; Eustace et al., 2013, 2016; Ritchie et al., 2015, 2016; Lacey et al., 2016). Hadal trenches do not form part of the continental shelf-slope-rise to abyssal plain continuum, but rather are deep and geographically sporadic clusters of disjunct and isolated environments.
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Present Address: School of Marine Science and Technology, Ridley Building, Newcastle University, Newcastle Upon Tyne NE1 7RU, UK.