Historical isolation and contemporary gene flow drive population diversity of the brown alga Sargassum thunbergii along the coast of China

Abstract

Background: Long-term survival in isolated marginal seas of the China coast during the late Pleistocene ice ages is widely believed to be an important historical factor contributing to population genetic structure in coastal marine species. Whether or not contemporary factors (e.g. long-distance dispersal via coastal currents) continue to shape diversity gradients in marine organisms with high dispersal capability remains poorly understood. Our aim was to explore how historical and contemporary factors influenced the genetic diversity and distribution of the brown alga Sargassum thunbergii, which can drift on surface water, leading to long-distance dispersal.

Results: We used 11 microsatellites and the plastid RuBisCo spacer to evaluate the genetic diversity of 22 Sargassum thunbergii populations sampled along the China coast. Population structure and differentiation was inferred based on genotype clustering and pairwise F _ST and allele-frequency analyses. Integrated genetic analyses revealed two genetic clusters in S. thunbergii that dominated in the Yellow-Bohai Sea (YBS) and East China Sea (ECS) respectively. Higher levels of genetic diversity and variation were detected among populations in the YBS than in the ECS. Bayesian coalescent theory was used to estimate contemporary and historical gene flow. High levels of contemporary gene flow were detected from the YBS (north) to the ECS (south), whereas low levels of historical gene flow occurred between the two regions.

Conclusions: Our results suggest that the deep genetic divergence in S. thunbergii along the China coast may result from long-term geographic isolation during glacial periods. The dispersal of S. thunbergii driven by coastal currents may facilitate the admixture between southern and northern regimes. Our findings exemplify how both historical and contemporary forces are needed to understand phylogeographical patterns in coastal marine species with long-distance dispersal.

Keywords: Gene flow; Historical isolation; Long-distance dispersal; Microsatellite; Plastid RuBisCo spacer; Population genetic diversity; Sargassum thunbergii.

Fig. 1

Two biogeographic patterns for intertidal species in Yellow-Bohai Sea and East China Sea. Lineage distribution and neighbor-joining tree were redrawn from (a) Sargassum horneri [4] and (b) Sargassum fusiforme [16]. Shaded sea areas are continental shelves that would have been exposed to the air during periods of low sea level. CDW: Changjiang diluted water. Blue line: the coastline of Jiangsu Province

Fig. 2

Haplotype distribution along the coast of China and median-joining network inferred from plastid rbc spacer data. Each line between main haplotypes represents one mutation step. Detailed locality information is shown in Table 1. Shaded sea areas are continental shelves that would have been exposed to the air during periods of low sea level. CCC: China Coastal Current; SCSWC: South China Sea Warm Current

Fig. 3

Clustering results of 22 S. thunbergii populations based on microsatellites, with K ranging from K = 2 to K = 5. Each individual is depicted by a vertical bar that is partitioned into colored sections. Population codes in parentheses are the same as in Table 1 and Fig. 2

Fig. 4

Principal Component Analysis (PCoA) based on microsatellites. The population codes are the same as in Table 1 and Fig. 2

Fig. 5

Estimates of contemporary (m) (a) and historical gene flow (N _m) (b) between S. thunbergii populations along the coast of China. Numbers above/below arrows represent migration rates in the direction of the arrow. The thickness of arrow is scaled according to the values. Population locations are shown in the map on the right