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Representative specimens of Athrotaxis showing the variation in shoot morphology of Athrotaxis selaginoides (top left images); samples from isolated individuals assigned to A. laxifolia (top center); A. cupressoides (top right) and individuals representing the range of forms present at Mt Read (bottom). All images are at the same scale.
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Premise of the study:
Homoploid hybrid speciation is receiving growing attention due the increasing recognition of its role in speciation. We investigate if individuals intermediate in morphology between the two species of the conifer genus Athrotaxis represent a homoploid hybrid species, A. laxifolia, or are spontaneous F1 hybrids.
Methods:
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... species -Th e putative parental species, Athrotaxis cupressoides and A. selaginoides , are monoecious, wind-pollinated evergreen conifers that are long-lived with individual stems capable of ex- ceeding 1000 yr in age ( Allen et al., 2011 ). Th ey are well-diverged in morphology, i.e., A. cupressoides has small scale-like leaves ap- pressed to the stem and ovulate cones with short bract scales, whereas A. selaginoides has spreading, keel-shaped leaves up to 12 mm long and elongated bract scales ( Fig. 1 ). Athrotaxis cupressoides occurs from 700-1400 m above sea level but usually from 1000 m to 1300 m ( Ogden, 1978 ) with a discontinuous distribution across the mountain ranges and plateaus of central, western, and southern Tasmania ( Fig. 2A ). ...
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... A. cu- pressoides , putative F 1 s, and advanced generation hybrids. Th e fi rst of these hybrid swarms was discovered by JRPW at Brumbys Creek in the Great Western Tiers (42 samples), the most eastern occurrence of all three taxa. Th e other was a large population (~1 km in diam- eter) with high morphological diversity at Mt Read (47 samples) ( Fig. 1 ) in the West Coast Range in western Tasmania ( Fig. 2C ...
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... spreading was measured qualitatively, on a scale of 1 to 14. A score of one indicated a tightly imbricate specimen while 14 indicated leaves spreading at an angle of approximately 70-80 ° from the stem ( Fig. 1 ). Morphological scores were summarized into a simple two dimensional space using nonmetric multidimensional scaling (NMDS) based on Bray- Curtis dissimilarity of standardized variables implemented in the soft ware package vegan ( Oksanen et al., 2013 ). ...
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... the deep divergence, we have found that rare hybridiza- tion between these species does occur. Th e morphologically inter- mediate plants that occur as isolated individuals within populations of the parent species ( Fig. 1 ), fi t precisely with F 1 s as predicted by the hybrid triangle plots and simulation analyses ( Fig. 7 ). In addi- tion, the distribution of alleles in these individuals is perfectly con- sistent with F 1 s-they are heterozygous at all loci, harboring alleles characteristic of both Athrotaxis selaginoides and A. cupressoides . ...
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... personal observation ). In addition, these F 1 -type individuals are rel- atively uniform in morphology, being more- or-less intermediate to A. cupressoides and A. selaginoides ( Figs. 1, 5 ). Th e Mt Read and Brumbys Creek popula- tions are clearly identifi ed as advanced gen- eration hybrid swarm populations. ...
Citations
... F2 hybrids can have variable but mostly lower heterozygosity. Unlike F2 hybrids, backcrosses are expected to be restricted to the sides of the triangle [39]. [20,22], while the remaining are frequently considered in studies addressing morphological variation in vipers (e.g., [15,40]). ...
Understanding how hybridization influences the morphology and fitness of hybrids is essential for studying adaptive evolution and ecological speciation. Secondary contact zones, where separately evolving populations meet and hybridize, offer valuable insights into the evolutionary processes driving speciation and provide an excellent system to address these questions. In this study, we investigate patterns of morphological and genetic variation of two congeneric viper species, Vipera aspis and V. latastei, across a contact zone in northern Spain (Oja-Tirón), where vipers with mixed morphology are often detected, but genetic studies addressing hybridization and relating patterns of genetic and morphological admixture are lacking. Using nine morphological traits (scalation and colouration) and 18 microsatellite markers, we (1) estimated the extent of hybridization, (2) morphologically characterized parental species and hybrids, and (3) evaluated the correlation between patterns of genetic and morphological admixture. Analyses revealed a bimodal hybrid zone with high rate of hybridization (22%) and prevalence of late-generation hybrids (F2 and backcrosses). Morphological analyses differentiated the two parental species, and a positive correlation (r = 0.95) was found between morphological and genetic patterns. The hybrid group displayed on average an intermediate morphology between the parentals, yet morphologically intermediate hybrids were rare in our dataset. Instead, most hybrids resembled the parental species with whom they share most of the genetic background. Notably, the hybrid group exhibited greater morphological variation than the parental groups. Traits with adaptative value, such as ventral scales and dorsal marks, showed significant differences between hybrids and the two parental species. Introgression of these traits may confer ecological advantages to hybrids, enhancing local adaptation. Overall, this study reveals a positive correlation between patterns of morphological and genetic variation across a hybrid zone and provides insights into the phenotypic consequences of hybridization on these viper species.
... Despite their distinct morphological traits and long recurrent hybrid origination, they do not initiate speciation. (Worth et al., 2016;Yu et al., 2023;Zhang et al., 2021). These cases highlight that conclusions about the large role of hybridization in speciation, at least as regards homoploid hybrids, as well as the time needed for their reproductive isolation, require further research. ...
Progressive changes in the environment are related to modifications of the habitat. Introducing exotic species, and interbreeding between species can lead to processes that in the case of rare species or small populations threatens their integrity. Given the declining trends of many populations due to increased hybridization, early recognition of hybrids becomes important in conservation management. Natural hybridization is prevalent in Jacobaea . There are many naturally occurring interspecific hybrids in this genus, including those between Jacobaea vulgaris and its relatives. Although Jacobaea erucifolia and J. vulgaris often co‐occur and are considered closely related, apart from the few reports of German botanists on the existence of such hybrids, there is no information on research confirming hybridization between them. Morphologically intermediate individuals, found in the sympatric distributions of J. vulgaris and J. erucifolia , were hypothesized to be their hybrids. Two molecular marker systems (nuclear and chloroplast DNA markers) were employed to test this hypothesis and characterize putative hybrids. Nuclear and chloroplast DNA sequencing results and taxon‐specific amplified fragment length polymorphism (AFLP) fragment distribution analysis confirmed the hybrid nature of all 25 putative hybrids. The AFLP patterns of most hybrids demonstrated a closer relationship to J. erucifolia , suggesting frequent backcrossing. Moreover, they showed that several individuals previously described as pure were probably also of hybrid origin, backcrosses to J. erucifolia and J. vulgaris . This study provides the first molecular confirmation that natural hybrids between J. vulgaris and J. erucifolia occur in Poland. Hybridization appeared to be bidirectional but asymmetrical with J. vulgaris as the usual maternal parent.
... Athrotaxis cupressoides is a very long lived (>1000 years), slow growing, endemic Tasmanian conifer (Ogden 1978;Allen et al. 2011). This species, as well as A. selaginoides, are the only extant species from the Athrotaxis genus, which is 150 million years old (a hybrid of the two species, A. laxifolia, also exists) (Worth et al. 2016a). Today, A. cupressoides is found in the alpine regions of central and western Tasmania, concentrated on the Central Plateau, which accounts for 76% of its total distribution (Harris and Kitchener 2005). ...
Athrotaxis cupressoides is an iconic Tasmanian palaeoendemic conifer that is vulnerable to fire. A survey of three populations burnt by severe fire in 2016, conducted 1 year post-fire, found 33% of stems were still alive, with many surviving stems suffering some canopy scorch. We re-surveyed these populations to quantify delayed mortality, resprouting, and presence of juveniles, and to determine whether fire impacts can be reliably assessed after 1 year. We applied three measures of fire severity: canopy scorched, canopy consumed, and the minimum burnt twig diameter of neighbouring shrubs. We found overall stem survival in 2020 was 31%, and that 97% of stems that were dead 4 years post-fire had died within the first year. Our best predictor of stem mortality was percentage canopy scorched. Overall, 1.8% of burnt stems resprouted, but severely burnt stems did not resprout. Juveniles were present ~9.9% of burnt trees in 2017, and only 1.8% in 2020. We conclude that A. cupressoides stems are not unusually fire sensitive, but rather, that the species’ vulnerability to severe fire results from its lack of reliable recovery mechanisms. This study shows that fire-caused mortality can be reliably assessed 1 year post-fire, and possibly earlier. Interventions such as sowing seed or transplanting seedlings could be necessary to re-establish fire-killed populations.
... Interspecific hybridization has played an essential role in plant evolution, and gene exchange between divergent species can result in new phenotypic or genetic diversity, adaptive variation, and, in some cases, contribute to speciation (Goulet et al., 2017). This process is more likely to happen between closely related species (Abbott et al., 2013; but also see Worth et al., 2016). Hybrid offspring production can promote gene exchange between parental species and, if the hybrids are fertile and can backcross with the parents, this may result in introgression that can lead to genetic swamping if gene exchange is excessive (Todesco et al., 2016) or introduce new, possibly adaptive, genetic combinations (Ellstrand et al., 2013). ...
Interspecific hybridization has been fundamental in plant evolution. Nevertheless, the fate of hybrid zones throughout the generations remains poorly addressed. We analyzed a pair of recently diverged, interfertile, and sympatric Petunia species to ask what fate the interspecific hybrid population has met over time. We analyzed the genetic diversity in two generations from two contact sites and evaluated the effect of introgression. To do this, we collected all adult plants from the contact zones, including canonicals and intermediary colored individuals, and compared them with purebred representatives of both species based on seven highly informative microsatellite loci. We compared the genetic diversity observed in the contact zones with what is seen in isolated populations of each species, considering two generations of these annual species. Our results have confirmed the genetic differentiation between the species and the hybrid origin of the majority of the intermediary colored individuals. We also observed a differentiation related to genetic variability and inbreeding levels among the populations. Over time, there were no significant differences per site related to genetic diversity or phenotype composition. We found two stable populations kept by high inbreeding and backcross rates that influence the genetic diversity of their parental species through introgression.
... Natural hybridization and polyploidy are two major evolutionary processes in plant speciation and diversification (Otto and Whitton 2000;Mable 2004;Ranney 2006;Abbott et al. 2013;Goulet, Roda, and Hopkins 2017). The frequency of both phenomena differs greatly between and within plant families (Ranney 2006;Wood et al. 2009;Marques et al. 2018). In conifers, polyploidy was reported to be rare, in contrast to natural hybridization that was found to be more frequent (Critchfield 1975;Ahuja 2005;Opgenoorth et al. 2010;Worth et al. 2016). ...
... The frequency of both phenomena differs greatly between and within plant families (Ranney 2006;Wood et al. 2009;Marques et al. 2018). In conifers, polyploidy was reported to be rare, in contrast to natural hybridization that was found to be more frequent (Critchfield 1975;Ahuja 2005;Opgenoorth et al. 2010;Worth et al. 2016). Nevertheless, a few cases of polyploidy have been reported in the genus Juniperus (Hall, Mukherjee, and Crowley 1973;Siljak-Yakovlev et al. 2010;Romo et al. 2013;Vallès et al. 2015). ...
Polyploidy and natural hybridization are considered as two major evolutionary processes involved in plant speciation and diversification. In conifers, natural hybridization has been noticed to be more frequent than polyploidy. Nevertheless, a few cases of polyploidy have been reported in the genus Juniperus. In this genus, a new variety Juniperus sabina var. balkanensis has been postulated to have arisen from an ancient hybridization between the tetraploid species Juniperus thurifera and the diploid species Juniperus sabina var. sabina. The genome size variation and the ploidy level of two J. sabina taxa were estimated by flow cytometry in a panel of 29 populations. All 13 populations of J. sabina var. sabina were diploid, with genome sizes ranging from 22.09 to 25.03 pg/2C, while the 16 populations of J. sabina var. balkanensis were tetraploid, with genome sizes ranging from 41.99 pg to 51.33 pg/2C. These findings open new venues towards the discovering of the polyploidization pathway of J. sabina var. balkanensis and to understand historical and ecological factors that explain its current geographical distribution.
... Clinal variation can theoretically be affected by neutral processes (Campitelli and Stinchcombe, 2013;Endler, 1973). In addition, many studies have reported significant correlations between morphological traits and the genetic status of hybrid individuals (Bergland et al., 2016;Minder et al., 2007;Worth et al., 2016), as well as the intermediate morphology of hybrid origin species (Rieseberg, 1997;Xing et al., 2014;Yakimowski and Rieseberg, 2014). The intermediate morphology and distribution range of A. sakawanum taxa between A. minamitanianum and A. costatum were shown in our previous study (Takahashi et al., 2018b). ...
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.
... The homoploid hybrid species A. sundingii and A. lemsii were intermediate between and distinct from the parental species based on leaf area and perimeter in particular. Argyranthemum sundingii and A. lemsii did not exhibit the high degree of variability between the parental species that one would associate with ongoing hybridisation and backcrossing (Tovar-Sánchez & Oyama 2004;Worth et al. 2016) conforming to the hypothesis that A. sundingii and A. lemsii are stabilised homoploid hybrid species as opposed to hybrid swarms. This finding, with broader sampling, corroborates the earlier work of Brochmann et al. (2000) who found the extent of morphological variation in the homoploid hybrid species was comparable to the parental taxa, whereas hybrid swarms and synthetic F2 hybrids exhibited a much wider range in variation. ...
Well‐characterised examples of homoploid hybrid speciation (HHS) are rare in nature yet they offer the potential to study a number of evolutionary processes. In this study we investigate putative homoploid hybrid species in the genus Argyranthemum (Asteraceae), a group of plants endemic to the Macaronesian archipelagos of the North Atlantic Ocean. We specifically address a number of knowledge gaps surrounding the origin(s) of A. sundingii and A. lemsii, which are thought to be derived from the same parental cross. Comparisons of leaf morphology suggest that A. sundingii and A. lemsii are distinct from their parental progenitors and distinguishable from each other based on leaf area. Ecological niche modelling (ENM) demonstrated that the homoploid hybrid species occupy novel habitats that are intermediate relative to the parental species. Nuclear SSRs and SNP data indicate that the homoploid hybrid species are distinct from the parental taxa, whilst population level sampling of chloroplast SSRs and Approximate Bayesian Computation show that A. sundingii and A. lemsii are independently derived from the same parental cross. As such, Argyranthemum represents an example of independent homoploid hybrid speciation events with evidence of divergence in leaf morphology and adaptation to novel intermediate habitats. On oceanic islands, which are often typified by steep ecological gradients and inhabited by recently derived species with weak reproductive barriers, multiple HHS events from the same parental cross are not only possible but are likely to have played a more important role in oceanic island radiations than we currently think.
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... However, recent molecular studies have demonstrated hybridization between deeply divergent plant (e.g. Worth et al. 2016) and animal species (e.g. Olave et al. 2011;2017a;Canestrelli et al. 2017). ...
Hybridization is likely to occur more often between closely related taxa that have had insufficient time to diverge to the point of reproductive incompatibility; hybridization between deeply divergent lineages is rare. In squamate reptiles, hybridization has been proposed as a possible explanation for the extensive paraphyly observed in mitochondrial gene trees in several species complexes of the South American lizard genus Liolaemus. One of the best‐documented cases is within the L. boulengeri and L. rothi complexes, which diverged ~5.5 million years ago. Here we describe a comprehensive study for approaching the hybridization hypothesis between these lizard species complexes. We explored the level of gene tree discordance using the novel “extra lineage contribution” statistics (XLC, presented in this study), that quantifies the level of gene tree discordance contribution per individual within a species. We included molecular data (12 nuclear and 2 mitochondrial genes) from 127 individuals, and results of a coalescent model‐based analysis show that the most likely explanation for the gene tree‐species tree discordance is interspecific hybridization. Our best‐supported hypothesis suggests current and past hybridization between L. rothi (rothi complex) and L. tehuelche (boulengeri complex), and independently between L. rothi and L. boulengeri and L. telsen (boulengeri complex). The hybrid descendants are characterized by intermediate phenotypes between the parental species, but are more similar to L. rothi in body size. We discuss the possible role of hybridization in Liolaemus evolution.
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... Argyranthemum sundingii andA. lemsii did not exhibit the high degree of variability between the parental species that one would associate with ongoing hybridisation and backcrossing (Tovar-Sánchez & Oyama, 2004;Worth et al., 2016) conforming to the hypothesis that A. sundingii and A. lemsii are stabilised homoploid hybrid species as opposed to hybrid swarms. This finding, with broader sampling, corroborates the earlier work of ...
The aim of this thesis was to investigate the evolutionary processes responsible for the diversification of the Macaronesian endemic genus Argyranthemum Webb (Asteraceae), using Next Generation Sequencing (NGS) methodologies. Transcriptome sequences from Macaronesian endemic genera, including Argyranthemum , were used to design primers for simple sequence repeat (SSR) markers. This was necessary to overcome the lack of genetic variation commonly observed in Macaronesian endemic lineages. Morphological, ecological and genetic analyses were then employed to address several unanswered questions surrounding the origin of two putative homoploid hybrid species, A. sundingii and A. lemsii . Specifically, each of the homoploid hybrid species are shown to be morphologically distinct, ecologically separated from their parental progenitors and independently derived from the same parental species. The hypothesis of independent homoploid hybrid speciation events facilitated by ecological isolation is supported by these results. Genotyping-By-Sequencing (GBS) was employed to investigate the processes associated with the diversification of Argyranthemum . The results of the phylogenetic and hybridisation analyses reveal that geographical isolation, habitat shifts and hybridisation have all contributed to the diversification of the group. In addition, morphological convergence has contributed to the diversification of the group. A study focussed on A. broussonetii reveals that the two subspecies (subsp. broussonetii and subsp. gomerensis ) are not closely related. Their morphological similarity is likely due to convergence as a result of their occupation of similar habitats. Finally, comparative transcriptomics was used to identify differentially expressed genes with a potential role in the ecological isolation and origin of the homoploid hybrid species in Argyranthemum . Although independently derived, A. sundingii and A. lemsii appear to have converged on similar expression phenotypes, likely a consequence of adaptation to similar habitats. NGS methodologies have revolutionised our ability to study the process of speciation in recently evolved lineages. Argyranthemum is the largest endemic genus of the Macaronesian archipelagos and an ideal model for investigating the processes responsible for diversification in oceanic island endemic lineages.
... Modern Sequoioideae is found only in the Northern Hemisphere, and comprises Sequoia, Sequoiadendron (both North American) and Metasequoia (native to east Asia). Conversely, extant Athrotaxidoideae comprises only three taxa, all endemic to Tasmania, Australia: Athrotaxis cupressoides, A. selaginoides D. Don and A. £ laxifolia Hook (a hybrid of the two aforementioned species; Isoda et al. 2000;Worth et al. 2016). These distributions need to be reconciled with the consistently close phylogenetic relationship of these subfamilies (Gadek et al. 2000;Farjon 2005;Mao et al. 2012;Yang et al. 2012;Shi et al. 2014; see 'phylogeny' section above). ...
The Tupuangi Flora of the Chatham Islands, New Zealand, reveals a south polar forest ecosystem, and important biogeographical links between eastern and western Gondwana. We employed neutron tomography (NT) to image fossil Cupressaceae seed cones from the Upper Cretaceous (Cenomanian) strata of the Tupuangi Formation. This technique facilitated the non-destructive ‘virtual extraction’ of three-dimensional, coalified specimens, whilst they were still embedded within a large volume of supporting silicate sedimentary rock. This study is the first reported application of NT in palaeobotanical taxonomy, and the combination of virtual and manual extraction techniques enabled a more complete treatment than would otherwise be possible if taxonomic data were limited to only one of these approaches. The seed cones were identified as Austrosequoia novae-zeelandiae (Ettingshausen) Mays & Cantrill comb. nov. In this case, NT data supplemented the compression fossil data by providing details such as the three-dimensional measurements of the gross morphology, and accurate estimations of bract-scale complex number. Furthermore, this technique appears to show promise in differentiating between organic compounds within an individual specimen. However, anatomical details and fine-scale morphology were indiscernible due to present limitations in spatial resolution. Austrosequoia novae-zeelandiae is interpreted as a stem group of Sequoioideae; it shares synapomorphic seed cone characters with extant sequoioids (e.g. Sequoia and Sequoiadendron), and plesiomorphic stomatal structures and leaf morphology. Abundant epiphyllous fungi (Plochmopeltinites sp.; Microthyriaceae) were also identified on the leaf cuticles of A. novae-zeelandiae. The high abundance of Austrosequoia in the Tupuangi Flora supports a cupressaceous floral province at south polar latitudes during the early Late Cretaceous. Furthermore, this stem group of Sequoioideae in eastern Gondwana during the early Late Cretaceous suggests an alternative, south-to-north dispersal route of sequoioids before the final continental separation of eastern and western Gondwana. © The Trustees of the Natural History Museum, London 2017. All rights reserved.
