Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters

Lilian Lieber,Graham Hall,Clinton Duffy,Deborah A Dawson,Chrysoula Gubili,S M Henderson ,Eleonora De Sabata,Mahmood S Shivji,Lucy A Hawkes,Emmett M Johnston ,David Sims ,Jackie Hall,Catherine S Jones,Simon Berrow,Matthew J Witt,Jane Sarginson,Sabine P Wintner,Malcolm P Francis ,Brendan J Godley,Philip D Doherty,Leslie R Noble

doi:10.1038/s41598-020-58086-4

Abstract

Migratory movements in response to seasonal resources often influence population structure and dynamics. Yet in mobile marine predators, population genetic consequences of such repetitious behaviour remain inaccessible without comprehensive sampling strategies. Temporal genetic sampling of seasonally recurring aggregations of planktivorous basking sharks, Cetorhinus maximus, in the Northeast Atlantic (NEA) affords an opportunity to resolve individual re-encounters at key sites with population connectivity and patterns of relatedness. Genetic tagging (19 microsatellites) revealed 18% of re-sampled individuals in the NEA demonstrated inter/multi-annual site-specific re-encounters. High genetic connectivity and migration between aggregation sites indicate the Irish Sea as an important movement corridor, with a contemporary effective population estimate (Ne) of 382 (CI = 241–830). We contrast the prevailing view of high gene flow across oceanic regions with evidence of population structure within the NEA, with early-season sharks off southwest Ireland possibly representing genetically distinct migrants. Finally, we found basking sharks surfacing together in the NEA are on average more related than expected by chance, suggesting a genetic consequence of, or a potential mechanism maintaining, site-specific re-encounters. Long-term temporal genetic monitoring is paramount in determining future viability of cosmopolitan marine species, identifying genetic units for conservation management, and for understanding aggregation structure and dynamics.

Highlights

Www.nature.com/scientificreports average more related than expected by chance, suggesting a genetic consequence of, or a potential mechanism maintaining, site-specific re-encounters
A minimum of 13 out of 22 microsatellite loci were successfully amplified in the 460 DNA samples screened, which included 394 samples from the Northeast Atlantic (NEA) collected over 6 years (2009–2014) and 66 samples opportunistically collected over 20 years from elsewhere in the world (MED = Mediterranean, NWA = Northwest Atlantic, PAC = New Zealand, SA = South Africa)
When Hardy Weinberg equilibrium (HWE) was assessed within global putative populations based on geographic origins, significant departures were identified for locus Cmax[07] in three out of nine populations

Summary

Introduction

Www.nature.com/scientificreports average more related than expected by chance, suggesting a genetic consequence of, or a potential mechanism maintaining, site-specific re-encounters. Gaining insight into repeated long-distance movement, its drivers and evolutionary consequences, is fundamental to understanding the ecology of these species It is central in evaluating current environmental concerns during an era of rapid climate change and extensive marine habitat modification, to inform the management and design of effective networks of marine protected areas (MPAs). The filter-feeding basking shark, Cetorhinus maximus, and the whale shark, Rhincodon typus, are the world’s largest fish Their horizontal movement is primarily driven by zooplankton dynamics and typically exceeds thousands of kilometres, precluding knowledge of natal origins and the potential existence of mating and breeding areas for either of these planktivores[3,4]. Identifying recurring spatial patterns, such as seasonal migration between distinct habitats or behavioural fidelity to ecologically important sites (feeding, breeding or mating areas) remains a challenge. Basking sharks forage selectively on zooplankton[13], and within the Northeast Atlantic (NEA) generally use deeper waters near shelf edges during winter, forming surface/temporal aggregations in shallower coastal waters during summer[14]

Methods

Results

Conclusion