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.