Fig 2 - available via license: Creative Commons Attribution 4.0 International
Content may be subject to copyright.
Source publication
The Amami Island group of the Ryukyu Archipelago, Japan, harbors extensive species diversity of Asarum in a small landmass. The fine-scale population genetic structure and diversity of nine insular endemic Asarum species were examined using nuclear DNA microsatellite loci and ITS sequences. High population genetic diversity (HS = 0.45–0.79) was est...
Contexts in source publication
Context 1
... floral morphology of the nine endemics is divergent in terms of size, color, calyx tube shape, calyx tube mouth size (throat), numbers of stamens and carpels, and pedicel length [35] (see S1 Table, Fig 2). For example, A. hatsushimae and A. leucosepalum develop long pedicels and flowers are arranged above ground, whereas the flowers of other species bloom on the ground. ...
Context 2
... example, calyx tube mouth size would be critical to select pollinator fauna: very narrow throat of Asarum gusk and A. pellucidum would limits pollinators to particular fauna with small body size such as mites or thrips, whereas wide throat of A. fudsinoi and A. lutchuense would be able to accept larger ones such as fungus gnat or amphipods inhabiting on forest floor. Most flowers conform to these morphologies as summarized in Fig 2 and S1 Table, suggesting a possibility of pollinator fauna differentiation among the species. ...
Similar publications
Aphids provide a good model system to understand the ecological speciation concept, since the majority of the species are host-specific, and they spend their entire lifecycle on certain groups of host plants. Aphid species that apparently have wide host plant ranges have often turned out to be complexes of host-specialized biotypes. Here we investi...
Citations
... (Gerdt Guenther Hatschbach, Brazilian botanist, 1923-2013; Ferreira da Silva & Ferraz de Oliveira 2008) as author of this manuscript name, even though on the actual specimens the name is attributed to "Hatus." or "Hats.", the former being the official abbreviation of Hatusima's surname (IPNI 2021), the latter another less commonly used abbreviation (e.g. Kokubugata et al. 2012;Matsuda et al. 2017). Unfortunately, this error was perpetuated in publications, with the name "Quintinia macrophylla Hatschb." ...
A new species of Quintinia A.DC. is described, Q. macrophylla Hatus. ex O.K.Paul, and the typifications of all other species occurring in New Guinea are reviewed. An identification key to all 13 species accepted for the area is provided, as well as an Appendix with a checklist of all species in the genus. Lectotypes are chosen for Quintinia altigena Schltr., Q. epiphytica Mattf., Q. lanceolata Reeder, Q. ledermannii Schltr., Q. macgregorii F.Muell., Q. nutantiflora Schltr., Q. pachyphylla Schltr. and Q. schlechteriana O.C.Schmidt.
... Unlike Asimitellaria spp., which appear to have only two types (and their intermediates) of pollinators and associated floral traits, pollination systems in Heterotropa are much more variable and species-specific (Okuyama unpublished data). Moreover, some sympatric species have been shown to be reproductively isolated despite their possible cross fertility, implying that differentiation in pollination systems is the basis of their isolating mechanism (Matsuda et al., 2017). Taken together, it is reasonable to consider that the diversification of the genus Asarum section Heterotropa in the Japanese archipelago would be an example of adaptive radiation. ...
The adaptive radiation of flowering plants as manifested by the floral diversity has long been considered associated with the diversity of plant–pollinator interactions, because changes in plant–pollinator interactions are hypothesized as one of the major mechanisms driving plant ecological speciation. To understand the relative contributions of various mechanisms for plant radiation, including pollinator changes, it is useful to study a plant group for which comparative study of the species life history across the whole lineage is feasible. To this end, we will focus on the plant lineages that have presumably radiated in the Japanese archipelago, namely, the genera Asimitellaria, Asarum, and Arisaema. By comparing these three genera, we will comment on the possible modes of adaptive radiation and diversification among the endemic flora of Japan. In this paper, we focus on the three plant lineages that have presumably radiated in the Japanese archipelago, namely, the genera Asimitellaria, Asarum, and Arisaema, in which detailed studies on phylogeny, reproductive isolation, and character evolution are underway. By comparing these three genera, we discuss the ecological mechanisms underlying the contrasting diversification modes among them.
... Heterotropa, most taxa inhabit almost the same environments (understory of warm temperate forests) and the floral difference and/ or geographic isolation would act as reproductive barriers rather than habitat differences. This insight was corroborated in a study of nine closely related Heterotropa taxa in the Amami islands, which are distributed in sympatry and/or close parapatry and morphologically different in floral traits (Matsuda et al., 2017). Thus, we considered that the divergence in flowering time and calyx tube width would have acted as one of the possible reproductive barriers in the six sister taxa pairs, and there are possibilities that the speciation triggered by trait differentiations may have also occurred in Heterotropa. ...
Aim
The Sino-Japanese Floristic Region has extremely high species diversity with respect to temperate plants; however, the reasons for this diversity are poorly understood because most studies have only considered geographic isolation caused by climatic oscillations. In some plant groups, high floral trait diversity and uneven species diversity between insular systems and the continental area suggest other factors may have important roles too. The primary purpose of this study is to reveal how abiotic and biotic factors have shaped the species diversity anomaly of Heterotropa between the insular systems and the continental area.
Location
The Sino-Japanese Floristic Region.
Taxon
Section Heterotropa (genus Asarum; Aristolochiaceae).
Methods
Using ddRAD-seq and chloroplast genome data, we built a time-calibrated phylogenetic tree including 79 species. We estimated the patterns of floral traits (flowering time and floral size) evolution using macroevolutionary modelling, and tested the correlation of speciation rate with the trait evolution rates. Finally, we estimated the isolation factors of all taxa pairs and sister-taxa pairs based on distribution range and floral traits.
Results
Phylogenetic analysis indicated that Heterotropa was diverged into two clades (continental clade and insular clade) in the Miocene, and the major subclades corresponded to geographic entities. Most rate shifts accelerating floral trait's evolution occurred during the Pleistocene period. Evolution rate of floral traits showed positive correlation with the speciation rate. Large proportion of taxa in the insular clade are distributed allopatrically. Several sister pairs showed floral trait divergence with geographic overlap.
Main Conclusions
The diversification of Heterotropa appears to have been triggered by geographic and climatic events, and subsequent repeated floral trait evolution with and without geographic isolation. Furthermore, the high species diversity in the insular systems would have been formed by the repeated range fragmentations and contractions. Our study demonstrates the importance of multidimensional studies to understand the diversification process of temperate plants in the Sino-Japanese Floristic Region.
... All species of Heterotropa, excluding two that are native to mainland China, are distributed in Japan and Taiwan; 49 species are endemic to the Japanese Archipelago . Heterotropa species are predominantly outcrossing (Sinn et al., 2015b;Matsuda et al., 2017), and their floral traits, including size, shape, color, and scent, are highly diversified (Azuma et al., 2010;Kakishima and Okuyama, 2018a), suggesting that pollinator interactions play a critical role in their diversification. Moreover, their pollination systems are considered to be a typical brood-site mimicry system wherein flowers provide no reward to their pollinators (Sugawara, 1988). ...
The sect. Heterotropa of the genus Asarum (Aristolochiaceae) comprises 49 endemic species in Japan. Species of Heterotropa are predominantly outcrossing and exhibit remarkable diversity in floral traits. This suggests that pollinator interactions may play critical roles in their diversification. A previous study found that A. tamaense did not produce seeds via autonomous self-pollination and was primarily pollinated by female individuals of a fungus gnat (Cordyla sp.; family Mycetophilidae) without providing any reward. Because the pollinator oviposits inside the calyx tube when visiting the flower, and the fungus gnat genus Cordyla is known to use mushrooms as brood sites, it has been hypothesized that the plant species adopts a mushroom mimicry system for pollination. Here, we revisited the floral biology of A. tamaense and investigated the hypothesized mushroom-mimicry system using time-lapse photography, pollinator identification via DNA barcoding, pollination experiments, and floral scent analyses. We confirmed that A. tamaense seldom sets fruit by autonomous self-pollination and that Cordyla sp. are likely the principal pollinators, as determined by DNA barcoding of adult insects that visited the flowers and eggs laid within the calyx tube. Cordyla sp. and other potentially pollinating dipteran species typically visited flowers from daytime to dusk. The major floral volatile compounds of A. tamaense were dimethyl disulfide that is a well-known major component of carrion scent, 2,3-butanediol diacetate, 2,3-butanediol, and several esters that are typical components of fermenting fruit scents. Although these volatile compounds are not typical in mushroom-mimicking flowers, it is possible that they are involved in attracting pollinators.
... Heterotropa, most taxa inhabit almost the same environments (understory of warm temperate forests) and the floral difference and/ or geographic isolation would act as reproductive barriers rather than habitat differences. This insight was corroborated in a study of nine closely related Heterotropa taxa in the Amami islands, which are distributed in sympatry and/or close parapatry and morphologically different in floral traits (Matsuda et al., 2017). Thus, we considered that the divergence in flowering time and calyx tube width would have acted as one of the possible reproductive barriers in the six sister taxa pairs, and there are possibilities that the speciation triggered by trait differentiations may have also occurred in Heterotropa. ...
The Sino-Japanese Floristic Region is highly diverse with respect to temperate plants. However, the reasons for this diversity are poorly understood because most studies have only considered geographic isolation caused by climatic oscillations. Heterotropa (genus Asarum; Aristolochiaceae) diverges here and shows high species diversity in insular systems (63 species) compared to continental areas (25 species). Heterotropa shows low dispersal ability with small distribution ranges, implying diversification by geographic events, and high floral diversity, implying pollinator-mediated diversification. To reveal how abiotic and biotic factors have shaped the diversity anomaly of Heterotropa, we conducted phylogenetic analysis using ddRAD-seq and chloroplast genome datasets including 79 species, estimation of floral trait evolution, and comparison of isolation factors within clades based on distribution range and floral trait analysis. Phylogenetic analysis indicates that Heterotropa originated in mainland China and expanded to the Japanese Archipelago in the Miocene, and the major clades almost correspond to geographic distributions. Floral traits evolved repeatedly in the tip nodes within the clades. Although the major clades include a high proportion of species pairs showing isolation by floral traits, there are no conditional relationships between two isolation factors, indicating that most species pairs with floral trait isolation are distributed allopatrically. The repeated exposure and submergence of land-bridges caused by climatic oscillations would have led to significant population fragmentation in insular systems. Thus, the diversity anomaly of Heterotropa would have resulted from geographic and climatic events during the Miocene, while subsequent repeated floral trait evolution would have followed geographic isolation during the Pleistocene.
... The species of the Amami clade grow either sympatrically or allopatrically in a variety of sloped forest floors along streams, on ridge-tops and in limestone areas. Matsuda et al. (2017) discovered that very little gene flow occurred among the four sympatric species on Amami-oshima Island (A. pellucidum, A. celsum, A. gusk and A. fudsinoi) despite the potential for cross-fertilization and very low genetic differentiation, indicating that mechanisms to reproductively isolate these species exist. Although the ecological basis of the origin and maintenance of species diversity in the Amami clade is unknown, it is likely that both pollination system and flowering phenology have played important roles, because each species has highly differentiated floral traits, including flowering seasons and floral colour, shape and scent (Matsuda et al., 2017;Y. ...
... Matsuda et al. (2017) discovered that very little gene flow occurred among the four sympatric species on Amami-oshima Island (A. pellucidum, A. celsum, A. gusk and A. fudsinoi) despite the potential for cross-fertilization and very low genetic differentiation, indicating that mechanisms to reproductively isolate these species exist. Although the ecological basis of the origin and maintenance of species diversity in the Amami clade is unknown, it is likely that both pollination system and flowering phenology have played important roles, because each species has highly differentiated floral traits, including flowering seasons and floral colour, shape and scent (Matsuda et al., 2017;Y. Okuyama, pers. ...
Background and aims:
The genus Asarum sect. Heterotropa (Aristolochiaceae) likely experienced rapid diversification into 62 species centred on the Japanese Archipelago and Taiwan, providing an ideal model for studying island adaptive radiation. However, resolving the phylogeny of this plant group using Sanger sequencing-based approaches has been challenging. To uncover the radiation history of Heterotropa, we employed a phylogenomic approach using double-digested RAD-seq (ddRAD-seq) to yield a sufficient number of phylogenetic signals and compared its utility with that of the Sanger sequencing-based approach.
Methods:
We first compared the performance of phylogenetic analysis based on the plastid matK and trnL-F regions and nuclear ribosomal ITS and phylogenomic analysis based on ddRAD-seq using a reduced set of the plant materials (83 plant accessions consisting of 52 species, 1 subspecies and 5 varieties). We also conducted more thorough phylogenomic analyses including the reconstruction of biogeographic history using comprehensive samples of 135 plant accessions consisting of 55 species, 1 subspecies, 8 varieties of Heterotropa, and 6 outgroup species.
Key results:
Phylogenomic analyses of Heterotropa based on ddRAD-seq were superior to Sanger sequencing-based approaches and resulted in a fully resolved phylogenetic tree with strong support for 72.0-84.8% (depending on the tree-reconstruction methods) of the branches. We clarified the history of Heterotropa radiation and found that A. forbesii, the only deciduous Heterotropa species native to mainland China, is sister to the evergreen species (core Heterotropa) mostly distributed across the Japanese Archipelago and Taiwan.
Conclusions:
The core Heterotropa group was divided into nine subclades, each of which had a narrow geographic distribution. Moreover, most estimated dispersal events (22 out of 24) were between adjacent areas, indicating that the range expansion has been geographically restricted throughout the radiation history. The findings enhance our understanding of the remarkable diversification of plant lineages in the Japanese Archipelago and Taiwan.
... The predicted historical interspecific gene flow across soil boundaries provides a more complex scenario than a simple allopatric speciation model, which has been discussed in several edaphic endemics, and highlights the relative importance of Pleistocene climatic oscillations for the evolution of serpentine plants and their distributional dynamics. Although interspecific gene exchange has the potential to eliminate species boundaries (Taylor et al. 2006), divergence in reproductive traits and habitat preferences between P. hidakana and P. takedana might be key factors for the maintenance and reinforcement of their species integrity, as has been discussed in other plant groups (Matsuda et al. 2017;Kay et al. 2018). However, latent effects against the speciation process and local adaptation of ultramafic Primula arising from interspecific hybridization across soil boundaries remain unclear. ...
Climatic perturbation during the Pleistocene era has played a major role in plant evolutionary history by altering species distribution range. However, the relative roles of climatic and geographic factors in the distribution dynamics remain poorly understood; in particular, the edaphic endemics. In this paper, we examine the evolutionary history of two ultramafic primroses, Primula hidakana and Primula takedana. These species are ecologically and morphologically distinct with disjunct distributions on Hokkaido Island, Japan. Primula hidakana is found on various rocks in southern Hokkaido and P. takedana in serpentine areas in northern Hokkaido. We performed population genetics analyses on nuclear and chloroplast data sets and tested alternative phylogenetic models of divergence using approximate Bayesian computation (ABC) analyses. Nuclear microsatellite loci clearly distinguished the two sister taxa. In contrast, chloroplast sequence variations were shared between P. takedana and P. hidakana. ABC analyses based on nuclear data supported a secondary contact scenario involving asymmetrical gene flow from P. hidakana to P. takedana. Paleodistribution modeling also supported the divergence model, and predicted their latitudinal range shifts leading to past secondary contact. Our findings highlight the importance of the distribution dynamics during the Pleistocene climatic oscillations in the evolution of serpentine plants, and demonstrate that tight species cohesion between serpentine and nonserpentine sister taxa has been maintained despite past interspecific gene flow across soil boundaries.
... Recent species divergence shows low genetic differentiation due to shared ancestral polymorphism and alleles not fixing within a population and/or a species (Pamilo and Nei, 1988;Linder and Rieseberg, 2004;Muir and Schlotterer, 2005;Krak et al., 2013;Pillon et al., 2013). In Japan, Asarum species seem to have diversified allopatrically in the Quaternary due to geographical fragmentation caused by climatic changes (Takahashi and Setoguchi, 2017;Matsuda et al. 2017). Asarum species take >7 years from sowing to first flowering and can live >20 years in wild populations (Kume, 1989(Kume, , 1993. ...
Background and aims:
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.
Methods:
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).
Key results:
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.
Conclusions:
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.
