Population Genomics and Lagrangian Modeling Shed Light on Dispersal Events in the Mediterranean Endemic Ericaria zosteroides (=Cystoseira zosteroides) (Fucales)

Lauric Reynes,Sandrine Ruitton,Myriam Valero,Charles-François Boudouresque,Didier Aurelle,Cristele Chevalier,Marc Verlaque,Stéphane Mauger,Stéphane Sartoretto,Aurélie Blanfuné,Thierry Thibaut,Christel Pinazo

doi:10.3389/fmars.2021.683528

Abstract

Dispersal is a central process that affects population growth, gene flow, and ultimately species persistence. Here we investigate the extent to which gene flow occurs between fragmented populations of the deep-water brown algae Ericaria zosteroides (Turner) Greville (Sargassaceae, Fucales). These investigations were performed at different spatial scales from the bay of Marseille (western Provence) to Corsica. As dispersal of zygotes is shown to be limited over distances beyond a few meters, we used a multidisciplinary approach, based on Lagrangian modeling and population genomics to test the hypothesis that drifting of fertile parts of thallus (eggs on fertile branches), mediated by ocean currents, enable occasional gene flow between populations. Therefore we assessed the respective contribution of oceanographic connectivity, geographical isolation, and seawater temperatures to the genetic structure of this species. The genetic structure was assessed using 10,755 neutral SNPs and 12 outlier SNPs genotyped by dd-RAD sequencing in 261 individuals of E. zosteroides. We find that oceanographic connectivity is the best predictor of genetic structure, while differentiation in outlier SNPs can be explained by the depth of populations, as emphasized by the minimum seawater temperature predictor. However, further investigations will be necessary for clarifying how depth drives adaptive genetic differentiation in E. zosteroides. Our analyses revealed that local hydrodynamic conditions are correlated with the very high divergence of one population in the Bay of Marseille. Overall, the levels of gene flow mediated by drifting were certainly not sufficient to counteract differentiation by local genetic drift, but enough to allow colonization several kilometers away. This study stresses the need to consider secondary dispersal mechanisms of presumed low dispersal marine species to improve inference of population connectivity.

Highlights

Genetic diversity is a prerequisite for the adaptive evolution of species
We will use the following definition of genetic connectivity: the degree to which the dispersal of individuals or propagules affect gene flow, with repercussions on evolutionary processes within populations, while demographic connectivity refers to the contribution of dispersal to the rate of population growth (Lowe and Allendorf, 2010)
Combining these indirect methods in a multidisciplinary approach was seen as an effective way to create the most complete picture of population connectivity, notably in marine species with low dispersal potential for which connectivity may be driven by unsuspected occasional long-distance dispersal events

Summary

INTRODUCTION

Genetic diversity is a prerequisite for the adaptive evolution of species. surveys of genetic diversity of rare and vulnerable species should be on the agenda of management and conservation frameworks (Hoban et al, 2020). Many organisms disperse through the release of many small propagules, which require the use of indirect methods such as genetic inference and/or Lagrangian models for assessing dispersal Combining these indirect methods in a multidisciplinary approach was seen as an effective way to create the most complete picture of population connectivity, notably in marine species with low dispersal potential for which connectivity may be driven by unsuspected occasional long-distance dispersal events (for review see Kinlan and Gaines, 2003). We conducted inference of genetic structure with RAD sequencing (dd-RADseq; Peterson et al, 2012) in a complementary way with Lagrangian modeling to unravel how gene flow is mediated by drifting of fertile parts of the thallus This multidisciplinary approach enabled us to answer the following questions: (i) Is E. zosteroides spatially structured at different spatial scales into genetically distinct populations? This multidisciplinary approach enabled us to answer the following questions: (i) Is E. zosteroides spatially structured at different spatial scales into genetically distinct populations? (ii) What is the respective influence of demography, oceanographic currents, and geographical distance on the genetic structure? (iii) Can we identify the sources of recruitment?

MATERIALS AND METHODS

RESULTS

DISCUSSION

DATA AVAILABILITY STATEMENT