Population genetic structure and genomic divergence in the Indo-West Pacific mangrove genus Rhizophor (Rhizophoraceae)

Abstract

Rhizophora species are the most widely distributed and the most representative mangrove trees in the Indo-West Pacific (IWP) region. Comparative studies of these species with shared life history traits can help identify evolutionary factors that have played most important roles in determining genetic diversity within and between populations in ocean-current dispersed mangrove tree species. In the first part of this study, 935 individuals from 54 natural populations were genotyped with 13 microsatellite markers to investigate the level of genetic variation, population structure, and gene flow on a broad geographic scale in Rhizophora apiculata, R. mucronata, and R. stylosa across the IWP region. In contrast to the pattern expected of long-lived woody plants with predominant wind-pollination, water-dispersed seeds and wide geographic range, genetic variation within populations was generally low in all the three species, especially in those peripheral populations from geographic range limits. Although the large water-buoyant propagules of Rhizophora have a capacity for long distance dispersal by ocean-current, such events might be rare in reality, as reflected by the low level of gene flow and high genetic differentiation between most of population pairs within each species. Historical vicariance, chronological fluctuation of sea level, land barriers (e.g. Malay Peninsula), and direction of oceanic current could all have influenced the connectivity among these populations. Given that mangrove species generally have small effective population sizes, it can be deduced that genetic drift coupled with limited gene flow have played a dominant role in producing the current pattern of genetic diversity and population structure in the IWP Rhizophora species, overshadowing the effects of their life history traits. Recent population fragmentation and disturbances arising from human activities could further endanger genetic diversity in mangrove trees. The microsatellite data of this study show that R. mucronata and R. stylosa are genetically close to each other and inseparable at some sympatric sites. The second part of this research investigated the genomic divergence, introgression, and speciation between R. mucronata and R. stylosa at three sites where the two species are sympatric using a large set of single nucleotide polymorphisms (SNPs) derived from restriction site associated DNA (RAD) sequencing to better understand species boundary between the two taxa. The genomic divergence between R. mucronata and R. stylosa was substantially high between sympatric populations in Southeast Asia. Regions with high genetic differentiation were widespread in the genome, inconsistent with the common expectation that a few “genomic islands of divergence” were responsible for the morphological and ecological divergences between closely related and hybridizing species. However, regions with much lower levels of genetic differentiation were found as well, albeit less frequently. Extensive introgression was found in the populations of R. stylosa in Australia, suggesting incomplete reproductive isolation between R. mucronata and R. stylosa. High levels of genomic divergence were found between Australian populations and Southeast Asian populations within both species, indicating deep historical separation between populations from these two regions and independent evolutionary history in different geographical locations.