Complementarity and discriminatory power of genotype and otolith shape in describing the fine-scale population structure of an exploited fish, the common sole of the Eastern English Channel

Marine Randon,Filip A M Volckaert,Elodie Réveillac,Kélig Mahé,Eric J Petit,Olivier Le Pape,Gilles Lassalle,Thomas Le Berre,Bruno Ernande,Johann Mourier

doi:10.1371/journal.pone.0241429

Abstract

Marine organisms show population structure at a relatively fine spatial scale, even in open habitats. The tools commonly used to assess subtle patterns of connectivity have diverse levels of resolution and can complement each other to inform on population structure. We assessed and compared the discriminatory power of genetic markers and otolith shape to reveal the population structure on evolutionary and ecological time scales of the common sole (Solea solea), living in the Eastern English Channel (EEC) stock off France and the UK. First, we genotyped fish with Single Nucleotide Polymorphisms to assess population structure at an evolutionary scale. Then, we tested for spatial segregation of the subunits using otolith shape as an integrative tracer of life history. Finally, a supervised machine learning framework was applied to genotypes and otolith phenotypes to probabilistically assign adults to subunits and assess the discriminatory power of each approach. Low but significant genetic differentiation was found among subunits. Moreover, otolith shape appeared to vary spatially, suggesting spatial population structure at fine spatial scale. However, results of the supervised discriminant analyses failed to discriminate among subunits, especially for otolith shape. We suggest that the degree of population segregation may not be strong enough to allow for robust fish assignments. Finally, this study revealed a weak yet existing metapopulation structure of common sole at the fine spatial scale of the EEC based on genotypes and otolith shape, with one subunit being more isolated. Our study argues for the use of complementary tracers to investigate marine population structure.

Highlights

Even in open habitats, populations of marine fish are commonly structured at relatively fine scales [1,2,3]
Mechanisms underlying the spatial structure of marine fish are (i) biophysical processes involved in egg and larval dispersal patterns [7,8] and (ii) post-larval movements related to homing vs straying behavior and migration strategies [9]
The paradigm suggesting that larval dispersal acts as the main driver of population structure and connectivity [7] has been revised such that a significant contribution of adult-mediated dispersal is acknowledged [10]

Summary

Introduction

Even in open habitats, populations of marine fish are commonly structured at relatively fine scales [1,2,3]. The degree of connectivity varies along a continuum of population segregation, from complete mixing (i.e. panmixia) to full isolation [4,5,6]. Populations of marine resources experience many pressures among which habitat degradation and fragmentation, fishing exploitation and climate change [11]. In such a context, the resilience of marine species relies on their dispersal capability throughout their life cycle [12]. From a fisheries perspective, understanding population connectivity and spatial structure is a prerequisite to sustainable exploitation. In case of mismatch between biological population and harvest stock unit (i.e. the spatial unit used for assessment and management), overexploitation or even collapse might dramatically arise [13,14,15,16]

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Conclusion