Aim
Although the evolution of island endemic plants has long been investigated, the majority of such studies have focused on species with remarkable levels of morphological variation and on islands ...substantially far from the mainland. Endemic plants on nearshore oceanic islands have received less attention. We investigate the population genetic structure and dynamics in plants endemic to nearshore and recently formed oceanic islands and examined the possibility of multiple colonizations onto the islands.
Location
Japanese mainland Honshu and the adjacent Izu Islands.
Taxon
Solidago virgaurea (Asteraceae).
Methods
Sixteen and nine populations of S. virgaurea complex were sampled from the mainland and islands respectively; phylogeographical and population genetics analyses, including Bayesian Phylogeographic and Ecological Clustering (BPEC) analysis and Discrete Phylogeographic Approach (DPA) to trace the history of colonization events onto the islands, were performed using plastid DNA and nuclear microsatellite DNA variations.
Results
Phylogenetically close plastid DNA haplotypes were shared between the mainland and islands, although the populations of S. virgaurea from different islands tended to exhibit phylogenetically distinct haplotypes. Admixture analyses based on nuclear DNA variations revealed distinct genetic structures between the mainland and island populations. Gene flow among islands is restricted but may partially offset genetic drift on each island.
Main conclusions
The genetic structure observed in this study may not have originated from a single dispersal event and successive expansion but rather from at least three colonization events and subsequent gene flow among island populations. Based on the nuclear DNA variations, the Izu Island populations of S. virgaurea are genetically distinct from the mainland ones. Repeated colonization events may have provided sufficient genetic diversity, which would generally be susceptible to founder effects and exert a driving force for evolutionary adaptation, to these oceanic island populations.
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•The wild-ginger, series Sakawanum shows clinal floral variation.•Evolutionary history of four taxa was inferred by molecular markers.•Two admixture events may have occurred between ...morphologically distinct taxa.•Geographic range shift to glacial refugia could have allowed secondary contact.•A complicated demographic history may have shaped intertaxonomic clinal variation.
Clinal variation is a major pattern of observed phenotypic diversity and identifying underlying demographic processes is a necessary step to understand the establishment of clinal variation. The wild ginger series Sakawanum (genus Asarum) comprises four taxa, which exhibit intertaxonomic clinal variation in calyx lobe length across two continental islands isolated by a sea strait. To test alternative hypotheses of the evolutionary history and to determine the implications for the formation of clinal variation, we conducted approximate Bayesian computation (ABC) analysis and ecological niche modeling (ENM). ABC analysis indicated that the scenario assuming multiple admixture events was strongly supported. This scenario assumed two admixture events occurred between morphologically distinct taxa, likely leading to the generation of intermediate taxa. One of the admixture events was estimated to have occurred during the last glacial maximum (LGM), during which the taxa were estimated to have formed a common refugia in southern areas by ENM analysis. Although four taxa are currently distributed allopatrically on different islands and trans-oceanic dispersal appears unlikely, the formation of a land bridge and the geographic range shift to refugia would have allowed secondary contact between previously isolated taxa. This study suggests that clinal variation can be shaped by demographic history including multiple admixtures due to climatic oscillations.
Abstract
Background and Aims
Hybridization is the main driver of plant diversification, and gene flow via hybridization has multifaceted effects on plant evolution. Carex angustisquama is an ...extremophyte that grows on soils heavily acidified by volcanism. Despite its habitat distinct from that of other species, this species is known to form interspecific hybrids, implying interspecific gene flow. It is crucial to verify the extent and direction of interspecific gene flow between C. angustisquama and closely related species to understand the evolutionary process of an extremophyte in solfatara fields.
Methods
In this study, expressed sequence tag–simple sequence repeat markers were utilized to infer the extent and direction of interspecific gene flow between C. angustisquama and closely related species.
Key Results
Bayesian clustering and simulation analyses revealed that all individuals of the three hybrid species were classified into the first hybrid generation or first backcross to C. angustisquama; therefore, current interspecific gene flow is limited. Moreover, in the Bayesian inference of historical gene flow based on multispecies samples, the model that assumed no interspecific gene flow was the most strongly supported across all species pairs, including phylogenetically close but ecologically distinctive species pairs.
Conclusions
Our results revealed that interspecific gene flow between C. angustisquama and its related species has been limited both currently and historically. Moreover, our results of Bayesian inference of historical gene flow indicated that extrinsic, rather than intrinsic, factors probably act as isolating barriers between Carex species, with hybrid breakdown via microhabitat segregation being the probable potential barrier. Overall, our findings provide insights into the evolutionary process of an extremophyte in solfatara fields and offer an important example of the mechanisms of diversification of the speciose genus Carex.
Climate relicts hold considerable importance because they have resulted from numerous historical changes. However, there are major interspecific variations among the ways by which they survived ...climate changes. Therefore, investigating the factors and timing that affected population demographics can expand our understanding of how climate relicts responded to historical environmental changes. Here, we examined herbaceous hydrangeas of genus Deinanthe in East Asia, which show limited distributions and a remarkable disjunction between Japan and central China. Chloroplast genome and restriction site-associated DNA sequencing revealed that speciation event occurred in the late Miocene (ca. 7-9 Mya) in response to global climate change. Two lineages apparently remained not branched until the middle Quaternary, and afterwards started to diverge to regional population groups. The narrow endemic species in central China showed lower genetic diversity (He = 0.082), as its population size rapidly decreased during the Holocene due to isolation in montane refugia. Insular populations in the three Japanese islands (He = 0.137-0.160) showed a genetic structure that was inconsistent with sea barriers, indicating that it was shaped in the glacial period when its range retreated to coastal refugia on the exposed sea floor. Demographic modelling by stairway-plot analysis reconstructed variable responses of Japanese populations: some experienced glacial bottlenecks in refugial isolation, while post-glacial range expansion seemingly exerted founder effects on other populations. Overall, this study demonstrated the involvement of not just one, but multiple factors, such as the interplay between climate changes, geography, and other population-specific factors, that determine the demographics of climate relicts.
East Asia's temperate deciduous forests served as sanctuary for Tertiary relict trees, but their ages and response to past climate change remain largely unknown. To address this issue, we elucidated ...the evolutionary and population demographic history of Cercdiphyllum, comprising species in China/Japan (Cercdiphyllum japonicum) and central Japan (Cercdiphyllum magnificum).
Fifty-three populations were genotyped using chloroplast and ribosomal DNA sequences and microsatellite loci to assess molecular structure and diversity in relation to past (Last Glacial Maximum) and present distributions based on ecological niche modelling.
Late Tertiary climate cooling was reflected in a relatively recent speciation event, dated at the Mio-/Pliocene boundary. During glacials, the warm-temperate C. japonicum experienced massive habitat losses in some areas (north-central China. north Japan) but increases in others (southwest/-east China, East China Sea landbridge, south Japan). In China, the Sichuan Basin and/or the middle-Yangtze were source areas of postglacial northward recolonization; in Japan, this may have been facilitated through introgressive hybridization with the cool-temperate C. magnificum.
Our findings challenge the notion of relative evolutionary and demographic stability of Tertiary relict trees, and may serve as a guideline for assessing the impact of Neogene climate change on the evolution and distribution of East Asian temperate plant.
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•The Japanese population diverged from the Eurasian population in the late Miocene.•Northern and Southern regional clades were identified in Japan.•Ecotypic taxa specialized in the ...various habitats belonged to the southern clade.•Phenotypic diversification occurred especially in the leading-edge populations.•Alpine and riverside ecotypic taxa appeared to have developed in parallel.
Phenotypic polymorphism within a species is a notable phenomenon in evolutionary biology to understand the process of adaptive speciation and other historical events. The Saxifraga fortunei complex is a widespread herb found in East Asia. It includes several ecotypic taxa corresponding to their habitat environments. The distribution of the various ecotypes in a limited area of the Japanese Archipelago makes the species a suitable model to investigate the impact of population demographic history and natural selection on lineage diversification. Here, Sanger-based sequencing was used to estimate the divergence timeframe between populations of the Eurasian continent and Japan. Genome-wide SNPs obtained by ddRAD sequencing were used to investigate the phylogeographic origins of ecotypic taxa. The phylogenetic analyses revealed the divergence of the Japanese population from the continental population in the late Miocene. Two distinct regional clades of North and South Japan were identified; phenotypic diversification was evident only in the southern clade. The South Japan clades displayed a historical distribution expansion from north to south. The phenotypic variations appeared to have generated during the expansion. The ecotypic boundaries were incongruent with the genetic grouping. We propose that morphological and ecological specialization in Japanese populations was repeatedly generated by local natural selection.
‘Living fossils’ are testimonies of long-term sustained ecological success, but how demographic history and natural selection contributed to their survival, resilience, and persistence in the face of ...Quaternary climate fluctuations remains unclear.
To better understand the interplay between demographic history and selection in shaping genomic diversity and evolution of such organisms, we assembled the whole genome of Cercidiphyllum japonicum, a widespread East Asian Tertiary relict tree, and resequenced 99 individuals of C. japonicum and its sister species, Cercidiphyllum magnificum (Central Japan).
We dated this speciation event to the mid-Miocene, and the intraspecific lineage divergence of C. japonicum (China vs Japan) to the Early Pliocene. Throughout climatic upheavals of the late Tertiary/Quaternary, population bottlenecks greatly reduced the genetic diversity of C. japonicum. However, this polymorphism loss was likely counteracted by, first, long-term balancing selection at multiple chromosomal and heterozygous gene regions, potentially reflecting overdominance, and, second, selective sweeps at stress response and growth-related genes likely involved in local adaptation.
Our findings contribute to a better understanding of how living fossils have survived climatic upheaval and maintained an extensive geographic range; that is, both types of selection could be major factors contributing to the species’ survival, resilience, and persistence.
Clines, the gradual variation in measurable traits along a geographical axis, play a major role in evolution and can contribute to our understanding of the relative roles of selective and neutral ...process in trait variation. Using genetic and morphological analyses, the relative contributions of neutral and non-neutral processes were explored to infer the evolutionary history of species of the series Sakawanum (genus Asarum), which shows significant clinal variation in calyx lobe length.
A total of 27 populations covering the natural geographical distribution of the series Sakawanum were sampled. Six nuclear microsatellite markers were used to investigate genetic structure and genetic diversity. The lengths of calyx lobes of multiple populations were measured to quantify their geographical and taxonomic differentiation. To detect the potential impact of selective pressure, morphological differentiation was compared with genetic differentiation (QCT-FST comparison).
Average calyx lobe length of A. minamitanianum was 124.11 mm, while that of A. costatum was 13.80 mm. Though gradually changing along the geographical axis within series, calyx lobe lengths were significantly differentiated among the taxa. Genetic differentiation between taxa was low (FST = 0.099), but a significant geographical structure along the morphological cline was detected. Except for one taxon pair, pairwise QCT values were significantly higher than the neutral genetic measures of FST and G'ST.
Divergent selection may have driven the calyx lobe length variation in series Sakawanum taxa, although the underlying mechanism is still not clear. The low genetic differentiation indicates recent divergence and/or gene flows between geographically close taxa. These neutral processes would also affect the clinal variation in calyx lobe lengths. Overall, this study implies the roles of population history and divergent selection in shaping the current cline of a flower trait in the series Sakawanum.
Geranium soboliferum
var.
kiusianum
and var.
hakusanense
(Geraniaceae) are believed to be relict plants that migrated southward from the Eurasian continent to the Japanese archipelago during the last ...glacial period.
G. soboliferum
var.
kiusianum
individuals and populations, which occur in wetlands in the Aso-Kuju region of Kyushu Island, are declining as a result of the deteriorating quality of the microhabitat, a process that is associated with the decrease in semi-natural grasslands. Using 10 polymorphic microsatellite markers, we evaluated the genetic diversity and population structure of the
G. soboliferum
complex, with the aim of understanding the species’ genetic characteristics to facilitate efficient conservation. Genetic demographic analysis suggested that Japanese
G. soboliferum
populations branched off from the Eurasian continental
G. soboliferum
var.
soboliferum
during the last glacial period and that, thereafter, the Japanese populations of the plant diverged into two lineages at the beginning of the Holocene epoch. The genetic diversity of
G. soboliferum
var.
kiusianum
was significantly lower than that of var.
hakusanense
, which is more widely distributed in central Honshu Island (mean
Ar
= 3.288 vs. 3.830 and
H
e
= 0.366 vs. 0.546). Genetic differentiation among populations was significantly higher (mean
F
ST
= 0.368 vs. 0.184) in var.
kiusianum
populations and, notably, exhibited non-significant patterns of isolation by distance, indicating that the populations underwent strong genetic drift independent of adjacent populations. Our findings suggested that the population’s isolation, and its associated habitat specialization and limited inter-population gene flow, would have accelerated genetic differentiation in var.
kiusianum
. Overall,
G. soboliferum
var.
kiusianum
, which is genetically unique to wetland habitats in the Aso-Kuju region, merits conservation, and appropriate human intervention and management are critical to maintaining its remaining habitats in semi-natural grasslands.
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