Divergent selection and historical geographic isolation drive lineage diversification and incipient ecological speciation in the gray mangroves of Arabia
In this study, we used the Arabian mangroves biological system to analyze the role of spatial environmental variation, geography and neutral evolution in driving population and lineage divergence. Phylogenetic analysis and demographic modeling revealed evolutionary relationships and times of population divergence consistent with periods of geographic isolation in glacial refugia both in the Red Sea and the PAG, ruling out the hypothesis of a postglacial colonization. Lineage split times were strikingly recent, providing evidence of an extremely fast process of diversification taking place within the enclosed water bodies around the Arabian Peninsula during the late Quaternary. Signs of adaptive divergence were conspicuous among lineages from the Red Sea, where demographic analysis detected no signals of migration among populations despite apparent absence of geographic barriers. Divergent genotype-environment association patterns observed for the Red Sea, along with high population differentiation and lack of migration, suggest that environmental differences may have been sufficient to constrain gene flow among populations, providing evidence of incipient ecological speciation. Ecologically-based constrains to gene flow can be due to selection against migrants, a process where dispersing individuals and hybrids suffer reduced fitness leading to limited gene exchange and habitat isolation among populations occurring in distinct environments (3, 53 ). Alternatively, the accumulation of differential adaptive changes may derive in the development of intrinsic barriers to gene flow among in Red Sea mangroves (3, 54 ). In sum, our results show a signal of positive correlation between neutral genetic structure and adaptive divergence among Red Sea mangrove populations occupying environmentally divergent habitats, congruently with a pattern of isolation-by-adaptation, an expected molecular signal in ecological speciation processes (3 ).
The distinct association patterns observed in the Red Sea contrast with differences in gene-environment correlation signals for populations of the PAG, which remained low even when comparing the northern and southern basins. Our analyses also detected potential ancestral and ongoing gene flow among populations. This suggests a lesser degree of adaptive differentiation within this region, where barriers to gene flow did not develop by adaptive divergence or by genetic drift in geographic isolation, either ancestral (in glacial refugia during low sea connectivity periods) or contemporary (between basins and with respect the Sea of Oman). Two main factors may have contributed to differences in the degree of adaptive divergence within the Red Sea and the PAG. First, times of divergence among population in the PAG are more recent than in Red Sea populations, dating back 3,600 and 6,700 generations in the latter versus 1,300 generations in the former. The arising of reproductive barriers among evolutionary lineages occurring either through differential selection or neutral differentiation is a time-dependent process, such that there may not have been sufficient time for divergence in the case of the PAG. Second, differential selection among PAG populations may have been weaker than in the Red Sea as a result of more limited environmental differences. Indeed, mangroves from the northern basin mostly occur in the warmest areas of the subregion, where differences with respect the southern basin are less pronounced (35, 52 ), suggesting a pattern of niche conservatism. Moreover, populations from the northern Red Sea and PAG showed similar genotype-environment association signals, a pattern of shared adaptive variability decoupled from inferred phylogenetic relationships that also suggests niche conservatism or perhaps evolutionary convergence. Populations from the less extreme environment of the Arabian Sea and Sea of Oman also showed distinctive patterns of gene-environment correlation, further supporting a process of adaptive differentiation among the main mangrove lineages of the Arabian Peninsula. Compared patterns of variation between Arabian mangroves, and especially those from the Red Sea and the PAG, reveal that high neutral genetic divergence and lineage diversity may arise in extremely short periods of time under specific selective and demographic conditions. In turn, ecological speciation requires of longer periods of reduced gene flow in geographic isolation and strong differential selection for reproductive barriers to develop, and to prevent gene exchange upon secondary contact. Overall, the results reported in this study support a process of fast lineage diversification driven by the combined factors of historical isolation and environmental selection, and emphasizes the potential of species’ range edges as promoters of speciation.