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Phylogenetic consequences of cytoplasmic gene flow in plants
Abstract and Figures
Abstract Despite the potential power and extensive use of DNA variation for phylogenctic reconstruction, it has become increasingly apparent that DNA phylogenies are often discordant with organismal phylogenies, Factors responsible for discordance include ...
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... Based on these results, phylogenetic incongruence between plastid and nuclear data (cytonuclear discordance) was detected in the deep clades of the WCS (Fig. 4). Cytonuclear discordance is commonly observed in some phylogenetically recalcitrant plant lineages [16,50,[78][79][80][81]; in most cases, nuclear phylogeny is more congruent with morphologic characteristics than plastid phylogeny, and such discordance is thought to be caused by hybridization [17,50,82,83]. ...
... The fossil evidence implies that ancient hybridization between Altingiaceae and closely related families might be feasible. Therefore, chloroplast capture [17,82] caused by ancient hybridization is likely a reasonable interpretation of the phylogenetic discordances detected in the deep relationships within the WCS. ...
Background The "woody clade" in Saxifragales (WCS), encompassing four woody families (Altingiaceae, Cercidiphyllaceae, Daphniphyllaceae, and Hamamelidaceae), is a phylogenetically recalcitrant node in the angiosperm tree of life, as the interfamilial relationships of the WCS remain contentious. Based on a comprehensive sampling of WCS genera, this study aims to recover a robust maternal backbone phylogeny of the WCS by analyzing plastid genome (plastome) sequence data using Bayesian inference (BI), maximum likelihood (ML), and maximum parsimony (MP) methods, and to explore the possible causes of the phylogenetic recalcitrance with respect to deep relationships within the WCS, in combination with molecular and fossil evidence. Results Although the four WCS families were identically resolved as monophyletic, the MP analysis recovered different tree topologies for the relationships among Altingiaceae, Cercidiphyllaceae, and Daphniphyllaceae from the ML and BI phylogenies. The fossil-calibrated plastome phylogeny showed that the WCS underwent a rapid divergence of crown groups in the early Cretaceous (between 104.79 and 100.23 Ma), leading to the origin of the stem lineage ancestors of Altingiaceae, Cercidiphyllaceae, Daphniphyllaceae, and Hamamelidaceae within a very short time span (∼4.56 Ma). Compared with the tree topology recovered in a previous study based on nuclear genome data, cytonuclear discordance regarding the interfamilial relationships of the WCS was detected. Conclusions Molecular and fossil evidence imply that the early divergence of the WCS might have experienced radiative diversification of crown groups, extensive extinctions at the genus and species levels around the Cretaceous/ Paleocene boundary, and ancient hybridization. Such evolutionarily complex events may introduce biases in topological estimations within the WCS due to incomplete lineage sorting, cytonuclear discordance, and long-branch attraction, potentially impacting the accurate reconstruction of deep relationships.
... Based on these results, phylogenetic incongruence between plastid and nuclear data (cytonuclear discordance) was detected in the deep clades of the WCS (Fig. 4). Cytonuclear discordance is commonly observed in some phylogenetically recalcitrant plant lineages [16,50,[78][79][80][81]; in most cases, nuclear phylogeny is more congruent with morphologic characteristics than plastid phylogeny, and such discordance is thought to be caused by hybridization [17,50,82,83]. ...
... The fossil evidence implies that ancient hybridization between Altingiaceae and closely related families might be feasible. Therefore, chloroplast capture [17,82] caused by ancient hybridization is likely a reasonable interpretation of the phylogenetic discordances detected in the deep relationships within the WCS. ...
Background
The “woody clade” in Saxifragales (WCS), encompassing four woody families (Altingiaceae, Cercidiphyllaceae, Daphniphyllaceae, and Hamamelidaceae), is a phylogenetically recalcitrant node in the angiosperm tree of life, as the interfamilial relationships of the WCS remain contentious. Based on a comprehensive sampling of WCS genera, this study aims to recover a robust maternal backbone phylogeny of the WCS by analyzing plastid genome (plastome) sequence data using Bayesian inference (BI), maximum likelihood (ML), and maximum parsimony (MP) methods, and to explore the possible causes of the phylogenetic recalcitrance with respect to deep relationships within the WCS, in combination with molecular and fossil evidence.
Results
Although the four WCS families were identically resolved as monophyletic, the MP analysis recovered different tree topologies for the relationships among Altingiaceae, Cercidiphyllaceae, and Daphniphyllaceae from the ML and BI phylogenies. The fossil-calibrated plastome phylogeny showed that the WCS underwent a rapid divergence of crown groups in the early Cretaceous (between 104.79 and 100.23 Ma), leading to the origin of the stem lineage ancestors of Altingiaceae, Cercidiphyllaceae, Daphniphyllaceae, and Hamamelidaceae within a very short time span (∼4.56 Ma). Compared with the tree topology recovered in a previous study based on nuclear genome data, cytonuclear discordance regarding the interfamilial relationships of the WCS was detected.
Conclusions
Molecular and fossil evidence imply that the early divergence of the WCS might have experienced radiative diversification of crown groups, extensive extinctions at the genus and species levels around the Cretaceous/Paleocene boundary, and ancient hybridization. Such evolutionarily complex events may introduce biases in topological estimations within the WCS due to incomplete lineage sorting, cytonuclear discordance, and long-branch attraction, potentially impacting the accurate reconstruction of deep relationships.
... This historical haplotype sharing may nevertheless explain why the reproductive barriers between species of the genus Betula remain permeable and blurred today, which is observed at the nuclear level with hybridization and introgression, and which supports the hypothesis of a syngameon composed notably of North American shrub birches. Chloroplast capture has been documented on several occasions in the scientific literature (Rieseberg & Soltis, 1991) and has been reported in other species and genera of angiosperms such as Populus deltoides (Godbout et al., 2019), Quercus spp. (Petit et al., 1993;Whittemore & Schaal, 1991) and Salix spp. ...
Arctic and subarctic ecosystems are rapidly transforming due to global warming, emphasizing the need to understand the genetic diversity and adaptive strategies of northern plant species for effective conservation. This study focuses on Betula glandulosa, a native North American tundra shrub known as dwarf birch, which demonstrates an apparent capacity to adapt to changing climate conditions. To address the taxonomic challenges associated with shrub birches and logistical complexities of sampling in the northernmost areas where species' ranges overlap, we adopted a multicriteria approach. Incorporating molecular data, ploidy level assessment and leaf morphology, we aimed to distinguish B. glandulosa individuals from other shrub birch species sampled. Our results revealed three distinct species and their hybrids within the 537 collected samples, suggesting the existence of a shrub birch syngameon, a reproductive network of interconnected species. Additionally, we identified two discrete genetic clusters within the core species, B. glandulosa, that likely correspond to two different glacial lineages. A comparison between the nuclear and chloroplast SNP data emphasizes a long history of gene exchange between different birch species and genetic clusters. Furthermore, our results highlight the significance of incorporating interfertile congeneric species in conservation strategies and underscores the need for a holistic approach to conservation in the context of climate change, considering the complex dynamics of species interactions. While further research will be needed to describe this shrub birches syngameon and its constituents, this study is a first step in recognizing its existence and disseminating awareness among ecologists and conservation practitioners. This biological phenomenon, which offers evolutionary flexibility and resilience beyond what its constituent species can achieve individually, may have significant ecological implications.
... In our plastome-based tree, G. mustelinum (AD4) and G. tomentosum (AD3) were resolved in an early diverging position on the same branch as sibling lineages, whereas in nuclear-genome-resolved trees G. tomentosum (AD3) resolved in an early branching position to the clade containing G. hirsutum (AD1), G. ekmanianum (AD6), and G. stephensii (AD7) (Yuan et al., 2021;Peng et al., 2022). Therefore, while G. tomentosum (AD3) may very well be more closely related to a clade of G. hirsutum (AD1), G. ekmanianum (AD6), and G. stephensii (AD7) when using nuclear data, G. tomentosum (AD3) appears to have retained a more ancestral version of the plastome possibly through plastid capture (Rieseberg & Soltis, 1991). In our analyses G. ekmanianum (AD6) and G. stephensii (AD7) resolved with wild G. hirsutum (AD1). ...
Cotton (Gossypium spp.) is a vital global source of renewable fiber and ranks among the world's most important cash crops. While extensive nuclear genomic data of Gossypium has been explored, the organellar genomic resources of allotetraploid cotton, remain largely untapped at the population level. The plastid genome (plastome) is well suited for studying plant species relationships and diversity due to its nonrecombinant uniparental inheritance. Here, we conducted de novo assembly of 336 Gossypium plastomes, mainly from domesticated cultivars, and generated a pan-plastome level resource for population structure and genetic diversity analyses. The assembled plastomes exhibited a typical quadripartite structure and varied in length from 160 103 to 160 597 bp. At the species level, seven allotetraploid species were resolved into three clades, where Gossypium tomentosum and Gossypium mustelinum formed an early diverging clade rooted by diploids, followed by splitting two sister clades of Gossypium darwinii-Gossypium barbadense and Gossypium hirsutum-Gossypium ekmanianum-Gossypium stephensii. Within the G. hirsutum clade the resolution of cultivated accessions was less polyphyletic with landrace and wild accessions than in G. barbadense suggesting some selection on plastome in the domestication of this adaptable species of cotton. The nucleotide diversity of G. hirsutum was higher than that of G. barbadense. We specifically compared the plastomes of G. hirsutum and G. barbadense to find mutational hotspots within each species as potential molecular markers. These findings contribute a valuable resource for exploring cotton evolution as well as in the breeding of new cotton cultivars and the preservation of wild and cultivated germplasm.
... Since our analysis did not incorporate chloroplast data, we were unable to further explore this phenomenon, thus providing support solely for the second scenario. Furthermore, it aligns with prior discussions emphasizing the reliability of nuclear data sets over plastid data in phylogenetic inference (Rieseberg & Soltis 1991). ...
Phylogenomics enhances our understanding of plant radiations in the biodiverse Andes. Our study focuses on Puya , primarily Andean and a part of the Bromeliaceae family. Using a phylogenomic framework based on the Angiosperms353 probe set for 80 species, we explored Puya ′s phenotypic evolution and biogeography. Divergence time analyses and ancestral area estimations suggested that Puya originated in Central Coastal Chile around 9 million years ago (Ma). Subsequently, it dispersed to the dry valleys of the Central Andes and Puna regions between 5–8 Ma, leading to the emergence of major lineages. Key events in the last 2–4 million years include the recolonization of Chilean lowlands and dispersal to the northern Andes via Peru's Jalcas, facilitating passage through the Huancabamba depression. This event gave rise to the high‐elevation Northern Andes clade. Using phylogenetic comparative methods, we tested the hypothesis that adaptation to the Andes' island‐like high‐elevation ecosystems was facilitated by unique leaf and floral traits, life history, and inflorescence morphology. Our findings suggest correlations between inflorescence axis compression, protective bract overlap, and high‐elevation living, potentially preventing reproductive structure freezing. Semelparity evolved exclusively at high elevations, although its precise adaptive value remains uncertain. Our framework offers insights into Andean evolution, highlighting that lineages adapted to life in dry ecosystems can easily transition to high‐elevation biomes. It also underscores how the island‐like nature of high‐elevation ecosystems influences phenotypic evolution rates. Moreover, it opens avenues to explore genetic mechanisms underlying adaptation to extreme mountain conditions.
... Then, the taxa in Clade 3 might have hybridized with those in Clade 1 or captured the cp from Clade 1, resulting in those taxa clustered into one clade (Clade 1 + 3) in the cpDNA phylogenetic trees. Chloroplast capture, a stochastic process that occurs in groups evolving through rapid radiation (the Asteraceae family is highly evolved and is in the stage of rapid differentiation), can influence cp genome (Rieseberg and Soltis, 1991;Bremer, 1994;Fior et al., 2013). Nevertheless, in the nrDNA tree, the samples of A. contorta and A. nepalensis were not clustered into the same main clade but rather clustered into Clade 1 and Clade 3, respectively, potentially reducing support for our hypothesis described above. ...
The HAP clade, mainly including Helichrysum Mill, Anaphalis DC., and Pseudognaphalium Kirp., is a major component of tribe Gnaphalieae (Asteraceae). In this clade, Anaphalis represents the largest genus of Asian Gnaphalieae. The intergeneric relationships among Anaphalis and its related genera and the infrageneric taxonomy of this genus are complex and remain controversial. However, there are few studies that have focused on these issues. Herein, based on the current most comprehensive sampling of the HAP clade, especially Anaphalis, we conducted phylogenetic analyses using chloroplast (cp) genome and nuclear ribosomal DNA (nrDNA) to evaluate the relationships within HAP clade, test the monophyly of Anaphalis, and examine the infrageneric taxonomy of this genus. Meanwhile, the morphological characters were verified to determine the circumscription and infrageneric taxonomy system of Anaphalis. Additionally, the biogeographical history, diversification processes, and evolution of crucial morphological characters were estimated and inferred. Our phylogenetic analyses suggested that Anaphalis is polyphyletic because it nested with Helichrysum and Pseudognaphalium. Two and four main clades of Anaphalis were identified in cp genome and nrDNA trees, respectively. Compared with nrDNA trees, the cp genome trees were more effective for phylogenetic resolution. After comprehensively analyzing morphological and phylogenetic evidence, it was concluded that the achene surface ornamentation and leaf base showed less homoplasy and supported the two Anaphalis lineages that were inferred from cp genome. Our biogeographical analyses based on cp genome indicated that HAP clade underwent rapid diversification from late Miocene to Pliocene. The two Anaphalis lineages appeared to have originated in Africa, then spread to Western and Southern Asia, and subsequently moved into Southwestern China forming a diversity center. The dispersal patterns of the two Anaphalis lineages were different. One dispersed around the world, except in Africa and South America. The other one dispersed to Eastern and Southeastern Asia from the ancestral origin region.
Interspecific hybridization in the genus Rosa (Rosaceae) is a common natural phenomenon. Hybrids often exhibit heterosis and new combinations of traits, which can provide raw materials for horticultural breeding. DNA barcodes and microsatellites have been proposed to facilitate species discrimination and hybrid detection. However, most SSR markers developed for roses have been found unapplicable to Rosa sect. Synstylae because of null alleles or failed amplification. In this study, we designed 15 pairs of microsatellite primers, along with four previously developed primers specifically for Rosa sect. Synstylae; we then analyzed 174 individuals of three closely related and sympatrically distributed Rosa species as a test case to evaluate the consistency between morphological and genetic hybrid identifications and to compare the discrimination efficiency of the DNA barcodes versus SSRs in detecting admixture. Principle coordinate analysis identified several individuals with intermediate phenotypes among the three rose species. Hybridization, intraspecific morphological polymorphism, and sample collection at different growth stages or phenological phases may have hindered species identification based on morphology and distorted the morphological clustering results. The molecular analyses showed that 12 (6.8%), 13 (7.4%), and 15 (8.6%) individuals were identified as admixed by STRUCTURE, NewHybrids, and nrITS sequences, respectively, of which only seven hybrids showed signs of admixture across all three methods. About 81% of the morphologically identifiable hybrids exhibited admixture based on SSRs. Meanwhile, approximately 69% of morphologically identifiable hybrids were detected, but four morphologically pure species individuals were identified as genetically admixed based on nrITS sequences. Some morphologically pure species individuals were genetically identified as hybrids while some morphological hybrids were identified as pure individuals based on certain molecular markers. Overall, EST-SSRs discriminated morphological hybrids more accurately than nrITS. We inferred that there is ongoing interspecific gene exchange among the three wild Rosa species that obscures morphospecies boundaries. Combining multiple data types and analytical approaches offers powerful utility for hybrid detection, regardless of the level of hybridization.
In this study of evolutionary relationships in the subfamily Rubioideae (Rubiaceae), we take advantage of the off-target proportion of reads generated via previous target capture sequencing projects based on nuclear genomic data to build a plastome phylogeny and investigate cytonuclear discordance. The assembly of off-target reads resulted in a comprehensive plastome dataset and robust inference of phylogenetic relationships, where most intratribal and intertribal relationships are resolved with strong support. While the phylogenetic results were mostly in agreement with previous studies based on plastome data, novel relationships in the plastid perspective were also detected. For example, our analyses of plastome data provide strong support for the SCOUT clade and its sister relationship to the remaining members of the subfamily, which differs from previous results based on plastid data but agrees with recent results based on nuclear genomic data. However, several instances of highly supported cytonuclear discordance were identified across the Rubioideae phylogeny. Coalescent simulation analysis indicates that while ILS could, by itself, explain the majority of the discordant relationships, plastome introgression may be the better explanation in some cases. Our study further indicates that plastomes across the Rubioideae are, with few exceptions, highly conserved and mainly conform to the structure, gene content, and gene order present in the majority of the flowering plants.
Dipelta Maxim. (Caprifoliaceae) is a Tertiary relic genus endemic to China, which includes three extant species, Dipelta floribunda, Dipelta yunnanensis , and Dipelta elegans . Recent progress in the systematics and phylogeographics of Dipelta has greatly broadened our knowledge about its origin and evolution, however, conflicted phylogenetic relationships and divergence times have been reported and warrant further investigation. Here, we utilized chloroplast genomes and population‐level genomic data restriction site‐associated DNA‐single nucleotide polymorphisms (RAD‐SNPs) to evaluate the interspecific relationships, population genetic structure and demographic histories of this genus. Our results confirmed the sister relationship between D. elegans and the D. yunnanensis – D. floribunda group, but with cyto‐nuclear phylogenetic discordance observed in the latter. Coalescent simulations suggested that this discordance might be attributed to asymmetric “chloroplast capture” through introgressive hybridization between the two parapatric species. Our fossil‐calibrated plastid chronogram of Dipsacales and the coalescent modeling based on nuclear RAD‐SNPs simultaneously suggested that the three species of Dipelta diversified at the late Miocene, which may be related to the uplift of the eastern part of Qinghai–Tibet Plateau (QTP) and adjacent southwest China, and increasing Asian interior aridification since the late Miocene; while in the mid‐Pleistocene, the climatic transition and continuous uplift of the QTP, triggered allopatric speciation via geographical isolation for D. floribunda and D. yunnanensis regardless of bidirectional gene flow. Based on both plastid and nuclear genome‐scale data, our findings provide the most comprehensive and reliable phylogeny and evolutionary histories for Dipelta and enable further understanding of the origin and evolution of floristic endemisms of China.
Restriction site variation in chloroplast DNA and nuclear ribosomal DNA was examined in 16 accessions from the Salicaceae comprising ten species of Populus and one outgroup species of Salix. Forty-nine restriction site mutations in the chloroplast DNAs were used to generate one most parsimonious phylogenetic tree. This tree indicates that all varieties of P. nigra (black poplars of sect. Aigeiros) have a chloroplast genome, maternally inherited, derived from the clade including the white poplars (P. alba and segregate species of sect. Populus) and divergent from the American cottonwoods of their own section. Twenty-one restriction site mutations in the nuclear ribosomal DNAs generated a single most parsimonious phylogenetic tree that indicates that the nuclear genome ofP. nigra is distinct from both the white poplars and American cottonwoods. The incongruity of these independent molecular phylogenies provides evidence for an unusual origin of the black poplars. Populus alba or its immediate ancestor acted as the maternal parent in a hybridization event with the paternal lineage of P. nigra. Subsequent backcrosses to the paternal species gave rise to the extant P. nigra with a chloroplast genome of P. alba and the nuclear genome of the paternal species. These hybridization and introgression events must have pre-dated the divergence of the black poplar varieties. The biphyletic nature of the P. nigra genomes suggests that dependency on one class of molecular or morphological markers or the merging of the two kinds of data sets to derive accurate estimates of true phylogenies could be misleading in plants.
Heiser (1949) hypothesized that a weedy race of Helianthus bolanderi had originated by the introgression of genes from H. annum into a serpentine race of H. bolanderi. Although Heiser's investigation of these species is frequently cited as one of the best examples of introgression in plants, definitive evidence of gene exchange is lacking (Heiser, 1973). To determine whether the weedy race of H. bolanderi actually originated via introgression, we analyzed allozyme, chloroplast-DNA (cpDNA), and nuclear-ribosomal-DNA (rDNA) variation.
Interspecific hybridization and introgression are important evolutionary processes in plants, but their full significance with respect to speciation at the diploid level remains unresolved. In this study, molecular markers from the plastid and nuclear genomes were used to document an unusual evolutionary history of Gossypium bickii Prokh. (Malvaceae). This species is one of three morphologically similar Australian cottons (along with G. austrate F. Muell. and G. nelsonii Fryx.) in section Hibiscoidea. In contrast to expectations based on previous morphological data, cladistic analysis of maternally inherited cpDNA restriction site mutations unites G. bickii with G. sturtianum J. H. Willis, a morphologically distant species in a different taxonomic section (Sturtia). Few restriction site mutations distinguish the plastomes of G. bickii and G. sturtianum, but these two cpDNAs are differentiated from those of G. australe and G. nelsonii by a minimum of 33 mutations (out of 640 sites scored). These two highly distinct clades are not supported by phylogenetic analyses of allozyme markers (from 58 populations) and restriction site mutations in nuclear ribosomal DNAs. Rather, phylogenies based on 83 nuclear markers indicate that G. bickii shares a more recent common ancestor with G. australe and G. nelsonii than it does with G. sturtianum. We suggest that the striking discrepancy between independent molecular phylogenies from two different genomes indicates a biphyletic ancestry of G. bickii. Our preferred hypothesis involves an ancient hybridization, in which G. sturtianum, or a similar species, served as the maternal parent with a paternal donor from the lineage leading to G. australe and G. nelsonii. Because we detected no G. sturtianum nuclear genes in G. bickii, we suggest that the nuclear genomic contribution of the maternal parent was subsequently eliminated from the hybrid or its descendent maternal lineage. Several possible mechanisms of cytoplasm transfer are suggested, including repeated backcrossing of the hybrid, as female, into the paternal donor lineage, selection against recombinant nuclear genomes and a form of apomixis known as semigamy. This example, and several others in Gossypium as well as other genera, attest to the evolutionary possibility of interspecific cytoplasmic transfer, and perhaps the origin of diploid species via reticulate speciation. In addition, this study offers an example of natural cytoplasmic introgression without long-term survival of nuclear genes from the maternal progenitor.
Enzyme electrophoresis and restriction-fragment analysis of chloroplast DNA (cpDNA) and nuclear ribosomal DNA (rDNA) were used to test the hypothesis that both Helianthus neglectus and H. paradoxus are stabilized hybrid derivatives of H. annuus and H. petiolaris. The four species are annuals, diploid outcrossers, and have the same chromosome number. Helianthus annuus and H. petiolaris had the same allele in highest frequency for 16 of the 18 isozyme loci examined and had different majority alleles for only 6-Pgd3 and Pgi2. The two species had divergent rDNAs that could be distinguished by seven diagnostic restriction site mutations and three length mutations, and their cpDNAs could be differentiated by three diagnostic restriction site mutations. The alleles observed in H. neglectus were not a combination of those observed in H. annuus and H. petiolaris. Although H. neglectus had only one unique allele, it possessed none of the three alleles specific to H. annuus. In contrast, it had four of the seven alleles specific to H. petiolaris. Furthermore, H. neglectus had the same rDNA type as H. petiolaris and had the same cpDNA as that found in two populations of H. petiolaris ssp. fallax. These data allowed us to speculate that H. neglectus may be a recent derivative of H. petiolaris ssp. fallax, rather than a stabilized hybrid derivative as originally proposed. In contrast, H. paradoxus combined the alleles of H. annuus and H. petiolaris and had no unique alleles. At Adh2, H. paradoxus was monomorphic for an allele found only in H. petiolaris ssp. fallax, whereas at 6-Pgd3 and Pgi2, it was monomorphic for high frequency H. annuus alleles. Furthermore, H. paradoxus combined the rDNA repeat types of both proposed parents and had the chloroplast genome of H. annuus. These data provide compelling evidence that H. paradoxus, in contrast to H. neglectus, was derived via hybridization.
Renewed interest in phylogenies over the last few decades coincides with a growing sense that it will actually be possible to obtain an accurate picture of evolutionary history. Indeed, the prospects of retrieving phylogeny now seem better than ever, owing to basic theoretical advance (due mainly to Hennig, 1966), the availability of computer programs that can handle large data sets, and the accessibility of new sources of evidence, especially molecular characters.