Aim Plants in islands have often evolved through adaptive radiation, providing the classical model of evolution of closely related species each with strikingly different morphological and ecological features and with low levels of genetic divergence. We emphasize the importance of an alternative (anagenetic) model of evolution, whereby a single island endemic evolves from a progenitor and slowly builds up genetic variation through time. Location Continental and oceanic islands. Methods We surveyed 2640 endemic angiosperm species in 13 island systems of the world, both oceanic and continental, for anagenetic and cladogenetic patterns of speciation. Genetic data were evaluated from a progenitor and derivative species pair in Ullung Island, Korea, and Japan. Results We show that the anagenetic model of evolution is much more important in oceanic islands than previously believed, accounting for levels of endemic specific diversity from 7% in the Hawaiian Islands to 88% in Ullung Island, Korea, with a mean for all islands of 25%. Examination of an anagenetically derived endemic species in Ullung Island reveals genetic (amplified fragment length polymorphism) variation equal or nearly equal to that of its continental progenitor. Main conclusions We hypothesize that, during anagenetic speciation, initial founder populations proliferate, and then accumulate genetic variation slowly through time by mutation and recombination in a relatively uniform environment, with drift and/or selection yielding genetic and morphological divergence sufficient for the recognition of new species. Low‐elevation islands with low habitat heterogeneity are highly correlated with high levels of anagenetic evolution, allowing prediction of levels of the two models of evolution from these data alone. Both anagenetic and adaptive radiation models of speciation are needed to explain the observed levels of specific and genetic diversity in oceanic islands.
We hypothesized that genetic consequences of oceanic-endemic plants derived via anagenesis would be quite different from those derived via cladogenesis. Populations of A. okamotoanum form a cluster and are clearly differentiated from A. mono, which suggests a single origin for the anagenetically derived island endemic. No pattern of geographical differentiation of populations occurs in A. okamotoanum, which supports the concept of initial founder populations diverging through time by accumulation of mutations in a relatively uniform environment without further specific differentiation.
This study reports the complete chloroplast (cp) DNA sequence of Eleutherococcus senticosus (GenBank: JN 637765), an endangered endemic species. The genome is 156,768 bp in length, and contains a pair of inverted repeat (IR) regions of 25,930 bp each, a large single copy (LSC) region of 86,755 bp and a small single copy (SSC) region of 18,153 bp. The structural organization, gene and intron contents, gene order, AT content, codon usage, and transcription units of the E. senticosus chloroplast genome are similar to that of typical land plant cp DNA. We aligned and analyzed the sequences of 86 coding genes, 19 introns and 113 intergenic spacers (IGS) in three different taxonomic hierarchies; Eleutherococcus vs. Panax, Eleutherococcus vs. Daucus, and Eleutherococcus vs. Nicotiana. The distribution of indels, the number of polymorphic sites and nucleotide diversity indicate that positional constraint is more important than functional constraint for the evolution of cp genome sequences in Asterids. For example, the intron sequences in the LSC region exhibited base substitution rates 5-11-times higher than that of the IR regions, while the intron sequences in the SSC region evolved 7-14-times faster than those in the IR region. Furthermore, the Ka/Ks ratio of the gene coding sequences supports a stronger evolutionary constraint in the IR region than in the LSC or SSC regions. Therefore, our data suggest that selective sweeps by base collection mechanisms more frequently eliminate polymorphisms in the IR region than in other regions. Chloroplast genome regions that have high levels of base substitutions also show higher incidences of indels. Thirty-five simple sequence repeat (SSR) loci were identified in the Eleutherococcus chloroplast genome. Of these, 27 are homopolymers, while six are di-polymers and two are tri-polymers. In addition to the SSR loci, we also identified 18 medium size repeat units ranging from 22 to 79 bp, 11 of which are distributed in the IGS or intron regions. These medium size repeats may contribute to developing a cp genome-specific gene introduction vector because the region may use for specific recombination sites.
Anagenetic speciation is an important mode of speciation in oceanic islands; one-fourth of the endemic plants are estimated to have been derived via this process. Few studies, however, have critically examined the genetic consequences of anagenesis in comparison with cladogenesis (involved with adaptive radiation). We hypothesize that endemic species originating via anagenetic speciation in a relatively uniform environment should accumulate genetic variation with limited populational differentiation. We undertook a population genetic analysis using nine nuclear microsatellite loci of Acer takesimense, an anagenetically derived species endemic to Ullung Island, Korea, and its continental progenitor A. pseudosieboldianum on the Korean Peninsula. Microsatellite data reveal a clear genetic distinction between the two species. A high F value in the cluster of A. takesimense was found by Bayesian clustering analysis, suggesting a strong episode of genetic drift during colonization and speciation. In comparison with A. pseudosieboldianum, A. takesimense has slightly lower genetic diversity and possesses less than half the number of private and rare alleles. Consistent with predictions, weak geographical genetic structure within the island was found in A. takesimense. These results imply that anagenetic speciation leads to a different pattern of specific and genetic diversity than often seen with cladogenesis.
Quercus acutissima (Fagaceae), a deciduous broad-leaved tree, is an important forest element in hillsides of South Korea. We used allozyme loci, Wright's F statistics, and multilocus spatial autocorrelation statistics to examine the distribution of genetic diversity within and among three local populations and the spatial genetic structure at a landscape scale (15 ha, 250 × 600 m) on Oenaro Island, South Korea. Levels of genetic diversity in Q. acutissima populations were comparable to mean values for other oak species. A moderate but significant deficit of heterozygotes (mean F(IS) = 0.069) was detected within local populations and low but significant differentiation was observed among populations (F(ST) = 0.010). Spatial autocorrelation analyses revealed little evidence of significant genetic structure at spatial scales of 100-120 m. The failure to detect genetic structure within populations may be due to intraspecific competition or random mortality among saplings, resulting in extensive thinning within maternal half-sib groups. Alternatively, low genetic differentiation at the landscape scale indicates substantial gene flow among local populations. Although wind-borne pollen may be the primary source of gene flow in Q. acutissima, these results suggest that acorn movement by animals may be more extensive than previously anticipated. Comparison of these genetic data for Oenaro Island with a disturbed isolated inland population suggests that population-to-population differences in internal genetic structure may be influenced by local variation in regeneration environment (e.g., disturbance).
We hypothesized that the main Korean mountain ranges provided many refugia for boreal plant species, where they likely found relatively stable habitats and maintained large population sizes. Under this scenario, high levels of genetic variation and low degree of differentiation among populations within these species were anticipated. To test this hypothesis, we examined levels of allozyme diversity (17 loci) in 12 populations of the common terrestrial montane orchid Oreorchis patens from the main ranges in Korea and 4 populations of its rare congener O. coreana, which is restricted to the Korean island of Jeju. As expected, O. patens harbored high levels of genetic variation within populations (%P = 62.8, A = 1.96, H (o) = 0.211, and H (e) = 0.237). Allele frequency differences among populations were low (F (ST) = 0.075), and the species also displayed a significant correlation between pairwise genetic differentiation and geographical distance. All these results suggest that extant populations were founded by multiple genetically diverse individuals and that most of this initial diversity would have been maintained in the stable mountainous conditions during Quaternary climatic oscillations. In contrast, we were unable to detect any genetic diversity in O. coreana, suggesting that contemporary populations likely originated from a single ancestral source population that had lost all genetic variability. From a long-term conservation genetics perspective, extreme rarity and small population sizes, coupled with its apparent genetic uniformity, place O. coreana at a high risk of extinction. Thus, both in situ and ex situ conservation efforts should be of particular importance for this species.
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