A Genome-Wide Approach to the Phylogeography of the Mussel Mytilus galloprovincialis in the Adriatic and the Black Seas

Marta Paterno,Levent Bat,Serge Planes,Emanuela Voutsinas,Giuseppe Guarnieri,Claudia Kruschel,Marina Panayotova,Aurore Chassanite,Ilaria Anna Maria Marino,Valentina Ruseva Todorova,Stefan Strungaru,Nataliya Milchakova,Leonardo Congiu,Vesna Mačić,Jamila Ben Souissi,Chiara Papetti,Elisa Boscari,Dragos Micu,Lorenzo Zane

doi:10.3389/fmars.2019.00566

Abstract

Connectivity between populations shapes the genetic structure of species being crucial for an effective management of environmental resources. Genetic approaches can provide indirect measures of connectivity, allowing the identification of genetically differentiated - unconnected - populations. In this study, we applied a 2b-RAD approach based on hundreds of polymorphic loci to provide the first detailed insight into the population genomics of the Mediterranean mussel Mytilus galloprovincialis in part of its native geographical range. We sampled 19 localities within the Mediterranean and Black Seas, and analyzed a total of 478 samples. We detected strong differences between the two seas, whereas no differences were found between samples from the Western and Central Mediterranean and within Western Mediterranean samples. In the Central Mediterranean a significant differentiation emerged comparing Central Adriatic samples with those from South Adriatic and Ionian Seas. Furthermore, an East-to-West genetic structuring was found in the Central Adriatic Sea, which was not present in the Southern Adriatic and Ionian Seas. These results possibly reflect the local oceanography, with a Middle Adriatic gyre unable to prevent genetic differentiation in this species, and a Southern Adriatic gyre that effectively mixes propagules in Southern areas. In the Black Sea, no signal of genetic structure was found, although samples were spaced at similar distances as in the Adriatic-Ionian area. Genetic connectivity patterns of M. galloprovincialis reveal peculiar species-specific features respect to other species with similar larval duration, suggesting caution in using genetic connectivity data of single species in defining conservation units. We recommend of using genetic connectivity data of many species representing a variety of life history traits, and we call for new investigations using high resolution population genomics, particularly in the Black Sea, to understand if areas separated by hundreds of kilometers can be considered genetically connected as mussels’ data suggest. This information will be critical to ensure “a well-connected system of protected areas” according to Aichi Target 11 of the Convention on Biological Diversity.

Highlights

Understanding the distribution of genetic variability is a keystone for environmental resources management and conservation biology of marine species (Moritz, 1994; Palumbi, 2003; Cowen et al, 2006)
Genetic Variability For the three datasets, similar values were obtained among the population samples for Ho, unbiased He and allelic richness (AR), confirmed by one-way ANOVA detecting no significant differences among samples (P > 0.05; Supplementary Tables S1–S3)
The genomic analysis of the 19 M. galloprovincialis populations sampled across different locations: (1) provided the first detailed analysis of the metapopulation structure of this species throughout part of its native range at the large scale; (2) allowed to investigate the presence of genetic differentiation at a smaller scale within basins; (3) enabled the comparisons with other CoCoNET species

Summary

Introduction

Understanding the distribution of genetic variability is a keystone for environmental resources management and conservation biology of marine species (Moritz, 1994; Palumbi, 2003; Cowen et al, 2006). Direct labeling and tracking of larvae is rarely a possibility (Levin, 1990; but see Becker et al, 2007), so genetic data are widely used for the indirect inference of population connectivity (Hellberg et al, 2002; Thorrold et al, 2002; Palumbi, 2003; Broquet and Petit, 2009; Cowen and Sponaugle, 2009; Lowe and Allendorf, 2010). A major task was the exploration of the population genetic structure of species from different taxonomic and functional groups having different ecological roles and dispersal modes. Multispecies genetic analysis is needed to obtain a “collection of networks of genetic variation of all species within a community” (Fortuna et al, 2009)

Methods

Results

Conclusion