Genetic diversity increases with depth in red gorgonian populations of the Mediterranean Sea and the Atlantic Ocean

PeerJ. 2019 May 24;7:e6794. doi: 10.7717/peerj.6794. eCollection 2019.

Abstract

Background: In the ocean, the variability of environmental conditions found along depth gradients exposes populations to contrasting levels of perturbation, which can be reflected in the overall patterns of species genetic diversity. At shallow sites, resource availability may structure large, persistent and well-connected populations with higher levels of diversity. In contrast, the more extreme conditions, such as thermal stress during heat waves, can lead to population bottlenecks and genetic erosion, inverting the natural expectation. Here we examine how genetic diversity varies along depth for a long-lived, important ecosystem-structuring species, the red gorgonian, Paramuricea clavata.

Methods: We used five polymorphic microsatellite markers to infer differences in genetic diversity and differentiation, and to detect bottleneck signs between shallow and deeper populations across the Atlantic Ocean and the Mediterranean Sea. We further explored the potential relationship between depth and environmental gradients (temperature, ocean currents, productivity and slope) on the observed patterns of diversity by means of generalized linear mixed models.

Results: An overall pattern of higher genetic diversity was found in the deeper sites of the Atlantic Ocean and the Mediterranean Sea. This pattern was largely explained by bottom temperatures, with a linear pattern of decreasing genetic diversity with increasing thermal stress. Genetic differentiation patterns showed higher gene flow within sites (i.e., shallow vs. deeper populations) than between sites. Recent genetic bottlenecks were found in two populations of shallow depths.

Discussion: Our results highlight the role of deep refugial populations safeguarding higher and unique genetic diversity for marine structuring species. Theoretical regression modelling demonstrated how thermal stress alone may reduce population sizes and diversity levels of shallow water populations. In fact, the examination of time series on a daily basis showed the upper water masses repeatedly reaching lethal temperatures for P. clavata. Differentiation patterns showed that the deep richer populations are isolated. Gene flow was also inferred across different depths; however, not in sufficient levels to offset the detrimental effects of surface environmental conditions on genetic diversity. The identification of deep isolated areas with high conservation value for the red gorgonian represents an important step in the face of ongoing and future climate changes.

Keywords: Atlantic Ocean; Climate change; Depth refugia; Genetic diversity; Mediterranean Sea; Paramuricea clavata.

Grant support

This study was supported by financial support to CESAM (UID/AMB/50017/2019), to FCT/MCTES through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. This study was also supported by a Pew Marine Fellowship (USA), the National Geographic Channel through project Deep Reefs, a National Geographic/Waitt grant (no. W153-11), the InAqua Conservation Fund (Oceanário de Lisboa), the European Regional Development Fund (COMPETE program) and the Foundation for Science and Technology (FCT) of Portugal through postdoctoral fellowship SFRH/BPD/111003/2015 and programs CCMAR/Multi/04326/2013, UID/MAR/04292/2013 and PTDC/BIA-BIC/114526/2009 (DiverseShores—Testing associations between genetic and community diversity in European rocky shore environments). Joanna Pilczynska was supported by a MARES Grant. MARES is a Joint Doctorate programme selected under Erasmus Mundus coordinated by Ghent University (FPA 2011-0016). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.