Long range gene flow beyond predictions from oceanographic transport in a tropical marine foundation species

Abstract

The transport of passively dispersed organisms across tropical margins remains poorly understood. Hypotheses of oceanographic transportation potential lack testing with large scale empirical data. To address this gap, we used the seagrass species, Halodule wrightii, which is unique in spanning the entire tropical Atlantic. We tested the hypothesis that genetic differentiation estimated across its large-scale biogeographic range can be predicted by simulated oceanographic transport. The alternative hypothesis posits that dispersal is independent of ocean currents, such as transport by grazers. We compared empirical genetic estimates and modelled predictions of dispersal along the distribution of H. wrightii. We genotyped eight microsatellite loci on 19 populations distributed across Atlantic Africa, Gulf of Mexico, Caribbean, Brazil and developed a biophysical model with high-resolution ocean currents. Genetic data revealed low gene flow and highest differentiation between (1) the Gulf of Mexico and two other regions: (2) Caribbean-Brazil and (3) Atlantic Africa. These two were more genetically similar despite separation by an ocean. The biophysical model indicated low or no probability of passive dispersal among populations and did not match the empirical genetic data. The results support the alternative hypothesis of a role for active dispersal vectors like grazers.

Figure 1

(a, b) Assignment of individuals to genetic groups that minimize Hardy–Weinberg and linkage disequilibria, estimated by STRUCTURE; colors depict the genetic subdivision based on K = 3 and K = 7 levels of subdivisions; Site names and coordinates are listed in Tables S1 and S4; (c) Sampling sites of Halodule wriightii with colors depicting the main highest genetic differentiation inferred with STRUCTURE (K = 3 groups); (d) Sample size (N); number of unique genotypes (G); genotypic richness, standardized allelic richness and standardized number of private alleles for the smallest common sample size. The figure was generated using R (version 4.2.2) and Inkscape 1.2.1 (https://inkscape.org/).

Figure 2

Genetic differentiation of populations of Halodule wrightii illustrated by factorial correspondence analysis (FCA). Distances in the plot are proportional to genetic divergence, illustrating that the divergence between the Gulf of Mexico and the other populations is much higher than that among any other populations.

Figure 3

Potential connectivity among Halodule wrightii populations that have been reported in literature and databases (see Table S5), estimated from simulations of transport by ocean currents data. The figure was generated using R (version 4.2.2).