Demographic inferences after a range expansion can be biased: the test case of the blacktip reef shark (Carcharhinus melanopterus)

Abstract

The evolutionary history of species is a dynamic process as they modify, expand, and contract their spatial distributions over time. Range expansions (REs) occur through a series of founder events that are followed by migration among neighboring demes. The process usually results in structured metapopulations and leaves a distinct signature in the genetic variability of species. Explicitly modeling the consequences of complex demographic events such as REs is computationally very intensive. Here we propose an an alternative approach that requires less computational effort than a comprehensive RE model, but that can recover the demography of species undergoing a RE, by combining spatially explicit modelling with simplified but realistic metapopulation models. We examine the demographic and colonization history of Carcharhinus melanopterus, an abundant reef-associated shark, as a test case. We first used a population genomics approach to statistically confirm the occurrence of a RE in C. melanopterus, and identify its origin in the Indo-Australian Archipelago. Spatial genetic modelling identified two waves of stepping-stone colonization: an eastward wave moving through the Pacific and a westward one moving through the Indian Ocean. We show that metapopulation models best describe the demographic history of this species and that not accounting for this may lead to incorrectly interpreting the observed genetic variation as signals of widespread population bottlenecks. Our study highlights insights that can be gained about demography by coupling metapopulation models with spatial modeling and underscores the need for cautious interpretation of population genetic data when advancing conservation priorities.

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Acknowledgements

We are grateful to the genotoul bioinformatics platform Toulouse Midi-Pyrenees (Bioinfo Genotoul) for providing computing resources (www.bioinfo.genotoul.fr). This work was funded by the Agence Nationale de la Recherche Demochips ANR-12-BSV7-0012, a LABEX CORAIL grant to SM and MV (CORALSHARK) and NSF Award DEB-01132229 to GN (Collaborative Research: Jaws and Backbone: Chondrichthyan Phylogeny and a Spine for the Vertebrate Tree of Life). We thank Ornella Weideli and Save Our Seas foundation for providing samples from the Seychelles. We also thank Andrew Chin, Jennifer Ovenden, Mark Meekan and Conrad Speed, Mael Imirizaldu, David Lecchini, Patrick Plantard, Jonathan Werry, Thomas Vignaud, Julia Spät and several students for providing samples or for assistance with blacktip reef shark population genetics sampling. We thank Johann Mourier, Andrea Manica, Anders Eriksson, Robert Beyer and Dave Swofford for helpful discussion.

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Correspondence to Stefano Mona.

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