High dispersal capacity and biogeographic breaks shape the genetic diversity of a globally distributed reef‐dwelling calcifier

• Published in: Ecology and evolution 2020-06, Vol.10 (12), p.5976-5989
• Main Authors: Prazeres, Martina, Morard, Raphaël, Roberts, T. Edward, Doo, Steve S., Jompa, Jamaluddin, Schmidt, Christiane, Stuhr, Marleen, Renema, Willem, Kucera, Michal
• Format: Article
• Language: English
• Subjects: Biogeography; Biological evolution; Calcification; Climate change; coral reefs; cryptic speciation; Deoxyribonucleic acid; Differentiation; Dispersal; Dispersion; DNA; Ecosystems; Evolutionary genetics; Genetic diversity; Genetic structure; Genotypes; Geographical distribution; Geology; Global warming; Heterogeneity; large benthic foraminifera; Lessepsian migrants; Niches; Original Research; phylogeography; Range extension; Species; Turnover rate
• ISSN: 2045-7758; 2045-7758
• DOI: 10.1002/ece3.6335

Understanding the role of dispersal and adaptation in the evolutionary history of marine species is essential for predicting their response to changing conditions. We analyzed patterns of genetic differentiation in the key tropical calcifying species of large benthic foraminifera Amphistegina lobifera to reveal the evolutionary processes responsible for its biogeographic distribution. We collected specimens from 16 sites encompassing the entire range of the species and analyzed hypervariable fragments of the 18S SSU rDNA marker. We identified six hierarchically organized genotypes with mutually exclusive distribution organized along a longitudinal gradient. The distribution is consistent with diversification occurring in the Indo‐West Pacific (IWP) followed by dispersal toward the periphery. This pattern can be explained by: (a) high dispersal capacity of the species, (b) habitat heterogeneity driving more recent differentiation in the IWP, and (c) ecological‐scale processes such as niche incumbency reinforcing patterns of genotype mutual exclusion. The dispersal potential of this species drives the ongoing range expansion into the Mediterranean Sea, indicating that A. lobifera is able to expand its distribution by tracking increases in temperature. The genetic structure reveals recent diversification and high rate of extinction in the evolutionary history of the clade suggesting a high turnover rate of the diversity at the cryptic level. This diversification dynamic combined with high dispersal potential, allowed the species to maintain a widespread distribution over periods of geological and climatic upheaval. These characteristics are likely to allow the species to modify its geographic range in response to ongoing global warming without requiring genetic differentiation. Genetic differentiation and distribution of populations can provide clues about processes shaping species evolutionary histories. We examined the genetic signature of globally distributed species of large benthic foraminifera in order to identify mechanisms acting at geological and ecological time scales. We found that while dispersal capacity allows populations to extend their range, geographic distribution was strongly shaped by biogeographic breaks and niche incumbency.