Amplicon sequencing of 42 nuclear loci supports directional gene flow between South Pacific populations of a hydrothermal vent limpet

Abstract

In the past few decades, population genetics and phylogeographic studies have improved our knowledge of connectivity and population demography in marine environments. Studies of deep‐sea hydrothermal vent populations have identified barriers to gene flow, hybrid zones, and demographic events, such as historical population expansions and contractions. These deep‐sea studies, however, used few loci, which limit the amount of information they provided for coalescent analysis and thus our ability to confidently test complex population dynamics scenarios. In this study, we investigated population structure, demographic history, and gene flow directionality among four Western Pacific hydrothermal vent populations of the vent limpet Lepetodrilus aff. schrolli. These vent sites are located in the Manus and Lau back‐arc basins, currently of great interest for deep‐sea mineral extraction. A total of 42 loci were sequenced from each individual using high‐throughput amplicon sequencing. Amplicon sequences were analyzed using both genetic variant clustering methods and evolutionary coalescent approaches. Like most previously investigated vent species in the South Pacific, L. aff. schrolli showed no genetic structure within basins but significant differentiation between basins. We inferred significant directional gene flow from Manus Basin to Lau Basin, with low to no gene flow in the opposite direction. This study is one of the very few marine population studies using >10 loci for coalescent analysis and serves as a guide for future marine population studies.

Subtle limits to connectivity revealed by outlier loci within two divergent metapopulations of the deep‐sea hydrothermal gastropod Ifremeria nautilei

“…For instance, Thaler et al (2011) showed that the gastropod Ifremeria nautilei is genetically differentiated between the Manus and North-Fiji/Lau basins. Similar results have been reported in other species, such as the limpet Lepetodrilus schrolli (Plouviez et al, 2019), the shrimp Rimicaris variabilis and the squat lobster Munidopsis lauensis (Thaler et al, 2014). Moreover, this latter species is characterized by additional intrabasin structuring.…”

“…schrolli (Plouviez et al, 2019) and A. boucheti (Breusing et al, 2021). Similarly to I. nautilei, L. schrolli is considered to possess lecithotrophic larvae (Berg, 1985;Craddock et al, 1997;Tyler et al, 2008).…”

Population connectivity of the hydrothermal-vent limpet Shinkailepas tollmanni in the Southwest Pacific (Gastropoda: Neritimorpha: Phenacolepadidae)

“…schrolli and squat lobster Munidopsis lauensis are probable lecithotrophic developers [see 63,64] and show genetic differentiation between Manus and Lau Basins (L. aff. schrolli) [10] or within Manus Basin (M. lauensis) [15]. This is not necessarily attributable to the general trend for marine invertebrates with lecithotrophic larvae to have shorter pelagic durations than planktotrophs [45,65].…”

“…The Southwest Pacific has been recognized as a single biogeographic province for deep-sea hydrothermal vent fauna based on its species composition [7,8]. Population connectivity of the component species has been well researched and documented among Manus (3˚S, 151˚E), North Fiji (16˚S, 173˚E) and Lau Basins (20˚S, 176˚E) (Fig 1) [9,10]. Different degrees of genetic connectivity have been shown for the vent-endemic species of mollusks and crustaceans in the three basins.…”

“…On the other hand, the confamilial snail Ifremeria nautilei has a local population in Manus Basin that is genetically distinct from those of North Fiji and Lau Basins [ 13 , 14 ]. Genetic differentiation has not been detected between the 1,100-km apart North Fiji and Lau Basins for any species examined [ 9 , 10 ], whereas 40 km-apart vent fields within Manus Basin harbor genetically isolated populations of the squat lobster Munidopsis lauensis [ 15 ]. Such differences in the levels of population structuring most probably reflect species-specific larval ecology and hence their dispersal capabilities in the presence of physical and hydrographic barriers [ 11 , 14 – 16 ].…”