Table of Contents

01 July 2022, Volume 60 Issue 4
Cover illustration: Paleo-Antarctic rainforest lineages migrated from Gondwana to the Asian tropics over tens of millions of years, but they are now threatened with geologically instantaneous extinctions. Top left, 52 million-year-old leafy branches of the podocarp conifer Dacrycarpus puertae from the Laguna del Hunco fossil lake beds (top right) in Chubut, Argentina. Bottom left, Dacrycarpus imbricatus foliage in primary rainforest, Kinabalu Park, Sabah, Malaysian Borneo. Bottom right, agricultu [Detail] ...
  
    Issue Information
  • Editorial
  • Song Ge and Jun Wen
    J Syst Evol. 2022, 60(4): 713-714.
    https://doi.org/10.1111/jse.12904

    The JSE established Awards of JSE Outstanding Papers in 2014 and has awarded two Outstanding Papers and two Outstanding Papers by Young Investigators each year since 2008 (Ge & Wen, 2015). The selection of the awards was based on votes and assessments from all 17 editors of the journal with the consideration of citation data from Web of Science and the impact on systematics and evolution. The winners of the Awards receive a certificate and a prize of $800 (JSE Outstanding Papers) or $500 (JSE Outstanding Papers by Young Investigators). Here, we are delighted to announce the four winners of the awards selected from JSE publications in 2020 and highlight the significance of these papers.

    JSE Outstanding Papers for 2020

    Wang et al. Major clades and a revised classification of Magnolia and Magnoliaceae based on whole plastid genome sequences via genome skimming

    As an early diverged lineage within the Magnoliids, the family Magnoliaceae is critical in systematic position on the Tree of Life and consists of many species with important values in timber production and traditional medicines, in addition to being ornamental plants. Nevertheless, the taxonomy and particularly the delimitations of genera and/or sections in this family have been highly controversial among taxonomists, with as few as two and as many as 17 genera. Wang et al. (2020) reconstructed the phylogeny of Magnoliaceae using sequences of the complete chloroplast genomes with a broad taxon sampling of 86 species. In conjunction with morphological and geographic evidence, they recognized two subfamilies Liriodendroideae and Magnolioideae, each with one genus (Liriodendron and Magnolia, respectively). Specifically, their results strongly supported 15 major clades within Magnolia s. l., inconsistent with the previous subgeneric treatment that recognized three subgenera. The authors further detected the data incongruence among several major clades and discussed the generic delimitation and phylogenetic relationships within the family. Overall, this work helps establish a better classification of Magnoliaceae and provides new insights into the global biogeographic diversification of this family with both temporal and tropical elements.

    Anderson & Song. Plant adaptation to climate change—Where are we?

    How plants adapt to globe climate change matters both for survival and extinction of plants and for agricultural and environmental sustainability and food security. In this review, Anderson & Song (2020) addressed (i) whether climate change exerted novel selection and disrupted local adaptation, (ii) how gene flow facilitated adaptive responses to climate change, and (iii) whether adaptive phenotypic plasticity could sustain populations in the short term. They also reviewed studies that tested the influence of climate change on species interactions, predicted the adaptive potential of plants under climate change, and dissected the genetic basis of plant adaptation to climate change. By highlighting several key research gaps, the authors encouraged additional applications of emerging genomic tools, along with interdisciplinary investigations, to enhance our ability to predict the adaptive potential of plants under climate change and to elucidate the genetic basis of complex trait variation.

    JSE Outstanding Papers by Young Investigators for 2020

    Song et al. Plastid phylogenomics improve phylogenetic resolution in the Lauraceae

    The family Lauraceae is a major component of tropical and subtropical forests worldwide, and includes many species that provide important economic products, including timber, perfume, spices, herbal medicines, and fruit crops. However, phylogenetic relationships within Lauraceae remain unsolved because of various reasons. Song et al. (2020) compiled a large data set that includes 43 newly sequenced and 77 downloaded plastomes representing 42 genera of Lauraceae and 17 related families of angiosperms. On this basis, they reconstructed the phylogenetic relationships within the Lauraceae and among seven of the nine families of the Laurales. In combination with the morphological evidence, the authors confirmed the monophyly of Lauraceae and identified nine monotypic clades that offered insights to improve the tribal classification of Lauraceae. They also described two new tribes (Caryodaphnopsideae and Neocinnamomeae) and updated the compositions of four other tribes. This study provides a robust phylogenetic framework through which to address the evolutionary history of the Magnoliids, the third-largest group of Mesangiospermae.

    Echeverría-Londoño et al. Dynamism and context-dependency in diversification of the megadiverse plant genus Solanum (Solanaceae)

    The uneven distribution of taxonomic diversity among the branches of the Tree of Life and geographic regions is one of the most intriguing puzzles in biology and has been hypothesized to arise from significant differences in the parameters governing rates of speciation and extinction. To address this issue, Echeverría-Londoño et al. (2020) assembled a set of time-calibrated and species-level phylogenies of extant Solanum species, including 1169 of its 1234 species, to reconstruct diversification rates across lineages and analyze them in a geographical context. They (i) explored the origins of the high heterogeneity of species richness among subclades of this genus, (ii) investigated the relative importance of clade-specific, tree-wide, and geographic variation in evolutionary rates, and (iii) analyzed how these patterns were associated with historical biogeographic movements of lineages and/or environmental changes. The results showed that the lineages in the Old World were diversifying more rapidly, which coincided with a long-distance dispersal event from the Neotropics to regions where major climatic changes were taking place. In addition, two separate groups of Solanum have migrated and established in Australia, with only the arid adapted lineages being significantly increased in diversification rate. Together, these findings provide a clear example of how successful colonization of new areas and niches could drive explosive diversifications.

    We want to congratulate the winners of the JSE Awards for their important contributions to systematics and evolution! We cordially invite the many colleagues in systematics and evolution to submit their first-rate research to JSE in the coming years.

  • Research Articles
  • Robert M. Kooyman, Sarah J. Ivory, Adam J. Benfield, and Peter Wilf
    J Syst Evol. 2022, 60(4): 715-727.
    https://doi.org/10.1111/jse.12853

    The Southeast Asian rainforest region is extremely complex and biodiverse. Fossils have shown that paleo-Antarctic rainforest lineages (PARLs) now extant in Asia tracked the ever-wet conditions needed to survive and diversify through deep time. However, the threat of future climate change to the remaining rainforest and PARLs in Southeast Asia has yet to be evaluated to set conservation priorities. We first quantified the woody-genus floristic relationships of Southeast Asian Island Groups by vetting and analyzing recent compilations of bioregional species data. We then evaluated the contributions to community assembly of woody fossil lineages and Island Group relationships to environmental gradients. To better understand climatic constraints of fossil lineage distributions and forecast distributions under projected future climate, we used exemplar living woody PARLs, including two angiosperms and two gymnosperms. Generalized linear models were used to project potential distributions under future climate pathways that assume no reduction in carbon dioxide emissions. The floristic analyses highlighted strong similarities among Island Groups in the ever-wet forest areas of Malesia, where PARLs are often concentrated. Ordination outliers represented more seasonal locations. Species distribution models showed that potential future distributions of ancient lineages are constrained by increasing rainfall seasonality and higher seasonal temperatures, with significant differences among exemplar genera. Notably, potential distributions often mapped onto de facto inaccessible areas, where forest clearing and the ubiquitous marine dispersal barriers that characterize the region will drastically inhibit potential relocation. These realities gravely threaten paleo-conservation values and contemporary rainforest community assembly processes in Southeast Asia.

  • Qiu-Yue Zhang, Min Deng, Yanis Bouchenak-Khelladi, Zhe-Kun Zhou, Guang-Wan Hu, and Yao-Wu Xing
    J Syst Evol. 2022, 60(4): 728-746.
    https://doi.org/10.1111/jse.12720

    Ulmaceae is a woody family widespread in northern temperate forests. Despite the ecological importance of this family, its phylogeny and biogeographic history are poorly understood. In this study, we reconstruct phylogenetic relationships within the family and infer spatio-temporal diversification patterns based on chloroplast genome (complete cpDNA) and nuclear ribosomal DNA sequences (nrDNA). The seven Ulmaceae genera are resolved in two main clades (temperate vs. tropical) by both cpDNA and nrDNA sequences. The temperate clade includes four genera, Hemiptelea, Zelkova, Planera, and Ulmus. The relationships among Planera and other genera are controversial because of inconsistent topologies between plastid and nuclear data. The tropical clade includes three genera ((Ampelocera, Phyllostylon), Holoptelea). Molecular dating and diversification analyses show that Ulmaceae originated in the Early Cretaceous (ca. 110–125 Ma) with the main lineages establishing from the Late Cretaceous to the early Eocene. The diversification rate slowed during the middle to the late Paleogene (ca. 23–45 Ma), followed by a rapid diversification of the East Asian temperate group in the Neogene, congruent with a global cooling event. The ancestral state optimization analysis suggests an East Asian origin of the temperate Ulmaceae clade during the Paleocene, which is consistent with the fossil record. Both phylogenomic and fossil evidence support East Asia as a center of origin and diversification for the temperate woody lineages.

    Temperate Ulmaceae clade originated in the Paleocene and then dispersed to other regions, therefore supporting the Out-of-Asia hypothesis. The East Asian temperate group diversified rapidly in the Neogene, congruent with a global cooling event. East Asia is a center of origin and diversification for the temperate woody lineages.
  • Yan-Ting Yang, Xu-Chen Yang, Ming-Cheng Wang, Lin-Ling Zhong, Rui Ma, Tao Ma, Jian-Quan Liu, Charles C. Davis, and Zhen-Xiang Xi
    J Syst Evol. 2022, 60(4): 747-758.
    https://doi.org/10.1111/jse.12725
    The development of next-generation sequencing technologies allows researchers to address complex problems in species delimitation, especially for non-model organisms. The taxonomic status of North American Nyssa species has long been debated and remains controversial. To elucidate the genetic structure and phylogenetic relationships of the five currently recognized North American Nyssa species, we conducted whole-genome sequencing of representative individuals and identified genome-wide single-nucleotide polymorphisms (SNPs) by utilizing the recently released chromosome-level assembly of Nyssa sinensis genome. Population genetic and phylogenetic analyses consistently inferred four well-supported genetic clusters from our sampled individuals, that is, N. aquatica, N. ogeche, N. sylvatica, and N. bifloraN. ursina. Although the identification of N. biflora and N. ursina is primarily based on the morphological characteristics of leaves and drupes, the present evidence, including our principal components analysis of leaf morphological traits, strongly supports the taxonomic designation of N. biflora and N. ursina as a single species. In addition, these four genetic clusters were grouped into two major clades, that is, clade 1 (N. aquatica and N. ogeche) and clade 2 (N. sylvatica and N. bifloraN. ursina). Despite the fact that no evidence of widespread gene flow was found between these two major clades, our analyses revealed the possibility of introgression from N. sylvatica into N. biflora, albeit at a relatively low frequency. This study demonstrates the use of whole-genome sequences as a promising avenue for delimiting species boundaries and further advocates for an integrative approach in the assessment of species delimitation.
    We conducted whole-genome sequencing of representative individuals for five currently recognized North American Nyssa species. Population genetic and phylogenetic analyses of genome-wide SNPs consistently inferred four well-supported genetic clusters, that is, Nyssa aquatica, N. ogeche, N. sylvatica, and N. bifloraN. ursina, and the recognition of N. biflora and N. ursina as a single species was also supported by PCA of leaf morphological characters. These four genetic clusters were further grouped into two major clades, that is, clade 1 (N. aquatica and N. ogeche) and clade 2 (N. sylvatica and N. bifloraN. ursina), and no evidence of widespread gene flow was found between the two major clades.
  • Lu Jiang, Qin Bao, Wei He, Deng-Mei Fan, Shan-Mei Cheng, Jordi López-Pujol, Myong Gi Chung, Shota Sakaguchi, Arturo Sánchez-González, Aysun Gedik, De-Zhu Li, Yi-Xuan Kou, and Zhi-Yong Zhang
    J Syst Evol. 2022, 60(4): 759-772.
    https://doi.org/10.1111/jse.12695
    Fagus L. is a key component in temperate deciduous broadleaf forests of the Northern Hemisphere. However, its biogeographic history has not been examined under the framework of a fully resolved and reasonably time-calibrated phylogeny. In this study, we sequenced 28 nuclear single/low-copy loci (18 555 bp in total) of 11 Fagus species/segregates and seven outgroups. Phylogenetic trees were reconstructed using both concatenation-based (maximum parsimony, maximum likelihood, and Bayesian inference) and coalescent-based methods (StarBEAST2, ASTRAL). The monophyly of two subgenera (Fagus and Engleriana) and most sections was well supported, except for sect. Lucida, which was paraphyletic with respect to sect. Longipetiolata. We also found a major phylogenetic conflict among North American, East Asian, and West Eurasian lineages of subgen. Fagus. Three segregates that have isolated distribution (F. mexicana, F. multinervis, and F. orientalis) were independent evolutionary units. Biogeographic analysis with fossils suggested that Fagus could have originated in the North Pacific region in late early Eocene. Major diversifications coincided with a climate aberration at the Eocene/Oligocene boundary and the global cooling since mid-Miocene. The late Miocene accelerated global cooling and the Pleistocene glaciations would have driven beeches into East Asia, North America, and West Eurasia. Meanwhile, range reduction and extinction in high latitudes, central Asia, and western North America converged to form the beech modern distribution pattern. This study provides a first attempt to disentangle the biogeographic history of beeches in the context of a nearly resolved and time-calibrated phylogeny, which could shed new insights into the formation of the temperate biome in the Northern Hemisphere.
    Fagus could have originated in the North Pacific region in late early Eocene. Both subgenera (Fagus and Engleriana) are monophyletic and they diverged at the Eocene/Oligocene boundary (32.7 Ma). The late Miocene accelerated global cooling and the Pleistocene glaciation would have driven beeches into East Asia, North America, and West Eurasia and most lineages split during this period.
  • Jia-Yu Xue, Shan-Shan Dong, Ming-Qiang Wang, Tian-Qiang Song, Guang-Can Zhou, Zhen Li, Yves Van de Peer, Zhu-Qing Shao, Wei Wang, Min Chen, Yan-Mei Zhang, Xiao-Qin Sun, Hong-Feng Chen, Yong-Xia Zhang, Shou-Zhou Zhang, Fei Chen, Liang-Sheng Zhang, Cymon Cox, Yang Liu, Qiang Wang, and Yue-Yu Hang
    J Syst Evol. 2022, 60(4): 773-788.
    https://doi.org/10.1111/jse.12708

    The early diversification of angiosperms is thought to have been a rapid process, which may complicate phylogenetic analyses of early angiosperm relationships. Plastid and nuclear phylogenomic studies have raised several conflicting hypotheses regarding overall angiosperm phylogeny, but mitochondrial genomes have been largely ignored as a relevant source of information. Here we sequenced mitochondrial genomes from 18 angiosperms to fill taxon-sampling gaps in Austrobaileyales, magnoliids, Chloranthales, Ceratophyllales, and major lineages of eudicots and monocots. We assembled a data matrix of 38 mitochondrial genes from 107 taxa to assess how well mitochondrial genomic data address current uncertainties in angiosperm relationships. Although we recovered conflicting phylogenies based on different data sets and analytical methods, we also observed congruence regarding deep relationships of several major angiosperm lineages: Chloranthales were always inferred to be the sister group of Ceratophyllales, Austrobaileyales to mesangiosperms, and the unplaced Dilleniales was consistently resolved as the sister to superasterids. Substitutional saturation, GC compositional heterogeneity, and codon-usage bias are possible reasons for the noise/conflict that may impact phylogenetic reconstruction; and angiosperm mitochondrial genes may not be substantially affected by these factors. The third codon positions of the mitochondrial genes appear to contain more parsimony-informative sites than the first and second codon positions, and therefore produced better resolved phylogenetic relationships with generally strong support. The relationships among these major lineages remain incompletely resolved, perhaps as a result of the rapidity of early radiations. Nevertheless, data from mitochondrial genomes provide additional evidence and alternative hypotheses for exploring the early evolution and diversification of the angiosperms.

    A detailed maximum-likelihood (ML) phylogram inferred from the nt data of 38 mt genes of 107 taxa. Asterisks indicate either bootstrap (BS) of 100% or posterior probabilities (PP) of 1.00. Maximum parsimony (MP), ML BS support values and Bayesian PP are labeled above nodes, respectively. Diamonds indicate BS of 100% and PP of 1.00 from all ML, MP, and Bayesian analyses. Asterisks indicate either BS of 100% or PP of 1.00. BS support values <50%, Bayesian PP <0.5, or incongruent topologies among ML, MP, and Bayesian inferences are indicated as “−.”
  • Chen-Yang Liao, Qing Gao, Deborah S. Katz-Downie, and Stephen R. Downie
    J Syst Evol. 2022, 60(4): 789-808.
    https://doi.org/10.1111/jse.12702
    Angelica is a taxonomically complex genus widespread throughout the North Temperate Zone. Previous phylogenetic studies of the genus have focused primarily on its East Asian species. The relationships among its North American members, the monophyly of these species, and the value of fruit morphology in circumscribing its taxa have yet to be examined. This study represents the most comprehensive sampling of Angelica to date (100 species) and includes all 26 species in North America. Relationships are inferred using Bayesian inference, maximum likelihood, and maximum parsimony analyses of ITS sequences and, for multiple accessions of each North American species, cpDNA ndhF-rpl32, rpl32-trnL, and psbM-psbD sequences. The fruit morphological characters examined were those considered phylogenetically important in East Asian Angelica. The results revealed that the North American species fell into three major clades: North American Angelica clade, Archangelica clade, and the Eurasian Angelica clade. Angelica dawsonii has affinities with Lomatium brandegeei. Fourteen species within the North American Angelica clade were strongly supported as monophyletic. Two paraphyletic species resulted in new combinations in A. lineariloba and A. venenosa. Conflict between the ITS-derived and cpDNA-derived phylogenies and the lack of resolution in portions of the trees may be due to chloroplast capture and rapid species radiation. Fruit morphology supported some interspecific relationships based on molecular data, and relationships revealed by ITS and cpDNA data were roughly in accordance with fruit classification type and geographic distribution region, respectively. A diagnostic key based on fruit morphology is provided for the identification of the North American Angelica taxa.
    The North American Angelica clade includes 26 species, of which 14 are monophyletic. Two paraphyletic species resulted in new combinations in A. lineariloba and A. venenosa. Relationships revealed by ITS and cpDNA data are roughly in accordance with fruit classification type and geographic distribution region, respectively.
  • Achyut Kumar Banerjee, Hai-Dan Wu, Wu-Xia Guo, Wei-Lun Ng, Wei-Xi Li, Yan Ma, Hui Feng, and Ye-Lin Huang
    J Syst Evol. 2022, 60(4): 809-823.
    https://doi.org/10.1111/jse.12746

    The phylogeography of coastal plant species is heavily influenced by past sealevel fluctuations, dispersal barriers, and life-history traits, such as long-distance dispersal ability of the propagules. Unlike the widely studied mangroves, phylogeographic patterns have remained mostly obscure for other coastal plant species. In this study, we sampled 42 populations of Scaevola taccada (Gaertn.) Roxb., a coastal shrub of the family Goodeniaceae, from 17 countries across its distribution range. We used five chloroplast DNA (cpDNA) and 14 nuclear microsatellite (simple sequence repeat [SSR]) markers to assess the influence of abiotic factors and population genetic processes on the phylogeographic pattern of the species. Geographical distribution of cpDNA haplotypes suggests that the species originated in Australia, followed by historical dispersal and expansion of its geographic range. Multiple abiotic factors, including the sealevel changes during the Pleistocene, the presence of landmasses like the Malay Peninsula, and contemporary oceanic circulation patterns, restricted gene flow between geographically distinct populations, thereby creating low haplotype diversity and a strong population structure. Population genetic processes acted on these isolated populations, leading to high nuclear genetic diversity and population differentiation, as revealed from analyzing the polymorphic SSR loci. Although genetic divergence was mostly concordant between cpDNA and SSR data, asymmetrical gene flow and ancestral polymorphism could explain the discordance in the detailed genetic structure. Overall, our findings indicate that abiotic factors and population genetic processes interactively influenced the evolutionary history and current phylogeographic pattern of S. taccada across its distribution range.

    Global phylogeography of the coastal shrub Scaevola taccada was assessed by genotyping 42 populations from 17 countries for 14 nuclear microsatellite and five chloroplast DNA markers. Our study revealed that wide distribution of the species was achieved by long-distance dispersal of the fruits. Pleistocene sealevel changes and contemporary ocean currents thereafter fragmented the distribution, and limited gene flow along with population genetic processes acting on these isolated populations shaped the current population genetic structure of the species. Genetic divergence was mostly concordant between marker types, although population structure was more prominent for chloroplast DNA and genetic differentiation was better explained by allele-size variations, supporting the use of multiple markers for deciphering phylogeographic patterns at a large spatial scale.
  • Perla Farhat, Sonja Siljak-Yakovlev, Oriane Hidalgo, Keith Rushforth, Jim A. Bartel, Nicolas Valentin, Ilia J. Leitch, and Robert P. Adams
    J Syst Evol. 2022, 60(4): 824-834.
    https://doi.org/10.1111/jse.12751

    While polyploidy (whole-genome multiplication) is generally considered rare in extant gymnosperms (with the exception of Ephedra, Ephedraceae), the occurrence of sporadic polyploid individuals belonging to various genera in the conifer family Cupressaceae has been reported in the literature. In addition, recent studies have revealed that polyploidy is not uncommon in the genus Juniperus (Cupressaceae), with tetraploid and hexaploid individuals reported in individuals collected from wild populations. Given these findings, we undertook a comprehensive screening of ploidy levels in 32 species belonging to the four genera that are phylogenetically closest to Juniperus (i.e., Callitropsis, Hesperocyparis, Xanthocyparis, and Cupressus), referred to as the CaHXCu complex. In addition, we also determined the ploidy level of two accessions in the poorly studied tetraploid, Fitzroya cupressoides. Using flow cytometry together with published chromosome counts to assign ploidy levels, we show that all species of the CaHXCu complex are diploid except Xanthocyparis vietnamensis, which is tetraploid, with a genome size of 44.60 pg/2 C. This study opens up new opportunities for studying the impact and consequences of polyploidy on the evolution and adaptation of species in Cupressaceae.

  • Zheng-Zhen Wang, Zi-Xiao Guo, Cai-Rong Zhong, Hao-Min Lyu, Xin-Nian Li, Norman C. Duke, and Su-Hua Shi
    J Syst Evol. 2022, 60(4): 835-847.
    https://doi.org/10.1111/jse.12709

    Subspecies is used to designate taxa below species but above geographical populations. What patterns of genomic variation are expected if taxa are designated as subspecies? In this study, we carry out such a survey on the mangrove tree Avicennia marina (Forssk.) Vierh. of the Indo-West Pacific coasts. This species has three subspecies, distinguished by morphological traits and geographical distribution. We collected samples from 16 populations (577 individuals) covering all three subspecies and sequenced 94 nuclear genes. We reveal comprehensive genetic divergence among subspecies, generally higher than among geographical populations within subspecies. The level of genetic diversity differs among the three subspecies, possibly hinting at a degree of separation among their gene pools. We observed that divergence varies from locus to locus across the genome. A small portion of the genome is most informative about subspecies delineation, whereas the rest is undifferentiated or slightly differentiated, hinting at uneven gene flow and incomplete isolation. The three subspecies likely split simultaneously with gene flow among lineages. This reticulate evolution results in some discordance between morphology and genetics in areas of population contact. In short, A. marina subspecies show species-like patterns in some respects and population-like patterns in others. We propose that the subspecies designated in A. marina are informative in predicting genetic divergences and useful in making conservation decisions.

    A comprehensive population genetic study on the mangrove tree Avicennia marina revealed substantial genetic divergence among its three phenotype-designated subspecies. Simulations indicate a trifurcate split of the three subspecies, followed by the pattern of reticulate evolution. The level of divergence varies from locus to locus across the genome, supporting the subspecies designation.
  • Lin-Bo Wang, Hong Ma, and Juan Lin
    J Syst Evol. 2022, 60(4): 848-858.
    https://doi.org/10.1111/jse.12712

    Gene duplication provides raw material for functional innovation, but gene duplicability varies considerably. Previous studies have found widespread asymmetrical sequence evolution between paralogs. However, it remains unknown whether the rate of evolution among paralogs affects their propensity of being retained after another round of whole-genome duplication (WGD). In this study, we investigated gene groups that have experienced two successive WGDs to determine which of two older duplicates with different evolutionary rates was more likely to retain both younger duplicates. To uncouple the measurement of evolutionary rates from any assignment of duplicate or singleton status, we measured the evolutionary rates of singleton genes in out-lineages but classified these singleton genes according to whether they are retained or not in a crown group of species. We found that genes that retained younger duplicates in the crown group of genomes were more constrained prior to the younger duplication event than those that failed to leave duplicates. In addition, we also found that the retained clades have more genes in out-lineages. Subsequent analyses showed that genes in the retained clades were expressed more broadly and highly than genes in the singleton clades. We concluded that the set of repeatedly retained genes after two WGDs is biased toward slowly evolving genes in angiosperms, suggesting that the potential of genes for both functional conservation and divergence likely affects their propensity of being retained after WGD in angiosperms.

    Phylogenomic analysis of 30 representative angiosperm species revealed that, in gene groups with two successive duplications, between two older duplicates, the clade retains both younger duplicates evolving at slower evolutionary rates and with relatively wider/higher levels of expression. This pattern can be found in relatively both old and recent whole-genome duplications (WGDs). In addition, we found that if a gene pair was retained in crown group genomes, the orthologous pair is also more likely to be retained in out-lineage species, suggesting that the potential of genes for both functional conservation and divergence likely affects their propensity of being retained after WGD in angiosperms. Above all, these results indicated that genes with multiple functions were more likely to be retained as duplicates again, and that the set of duplicated genes is biased has important implications for genome-scale studies.
  • Xiao He, Jing-Jing Cao, Wei Zhang, Yong-Quan Li, Chao Zhang, Xiao-Hong Li, Guo-Hua Xia, and Jian-Wen Shao
    J Syst Evol. 2022, 60(4): 859-875.
    https://doi.org/10.1111/jse.12726

    An accurate understanding of species diversity is essential to studies across a wide range of biological subdisciplines. However, species delimitation remains challenging in evolutionary radiations, particularly in those herbaceous plants associated with microendemic, naturally fragmented distribution systems, where genotypic and phenotypic traits likely evolved discordantly. The Primula merrilliana complex, which is endemic to eastern China and has high horticultural value, used to be treated as one species but several clues suggested it might be composed of multiple species. Here we used multiple lines of evidence, including molecular, morphological, reproductive isolation, and geographic data, to assess independently evolving lineages within this complex. Our results indicated that the species diversity in the complex was underestimated previously, and four species (independently evolving lineages) can be recognized, including two new species described here. The extensive variation of the breeding system, especially the floral morph transition from distyled (outcrossing) to homostyled (selfing) multiple times, possibly promoted the rapid speciation within such a small geographic scale. This study case indicated that the phenomenon of genetically highly divergent but morphologically indistinguishable is perhaps shown in herbs with fragmented distributions; the alternative extreme evolutionary phenomenon, in which complete reproductive barriers have been accumulated but with little genetic differentiation, also exists. Thus we highlight the importance of incorporating other characters, such as postzygotic reproductive isolation and geographic data, with commonly used molecular and morphological traits to infer species boundaries through an integrative taxonomic approach in such systems.

    An accurate understanding of species diversity is essential to studies across a wide range of biological subdisciplines. Here, based on integrating molecular, morphological, reproductive isolation, and geographic data, we found there are four species, that is, Primula merrilliana, P. qiupuensis, P. wannanensis sp. nov., and P. zhexiensis sp. nov., in the P. merrilliana complex, which is endemic to a narrow area (<6000 km2) in southern China.
  • Qing-Hua Wang, Shan-Shan Dong, Jin-Long Zhang, Yang Liu, and Yu Jia
    J Syst Evol. 2022, 60(4): 876-900.
    https://doi.org/10.1111/jse.12713

    Orthotrichum Hedw. s.l. and Ulota Mohr s.l. are two of the most speciose genera of the xerophytic moss family Orthotrichaceae. We reconstructed the phylogeny of these two genera using three data matrices: (i) organellar genomes and 33 taxa; (ii) six loci from three genomes and 144 taxa; and (iii) two plastid loci and 163 taxa. The present phylogeny, based on the maximum sampling of genes or taxa to date, generally confirms the new classification of Orthotrichum and Ulota, and indicated that all Ulota species, except Ulota phyllantha Brid., form a clade and three lineages comprise the cryptoporous Orthotrichum clade. We provided new morphological characters that support the present division of the two genera. Ancestral state reconstruction of stoma indicates that superficial stomata in Orthotrichum represent a plesiomorphic character and semi-immersed stomata were derived from immersed stomata. The results also suggest that immersed stomata independently arose once in Orthotrichum, whereas semi-immersed stomata probably arose more than once. Molecular dating analysis reveals that the occurrence of immersed stomata is probably related to arid environments during the early Oligocene to late Miocene, whereas the appearance of semi-immersed stomata might be associated with the mesic–xeric or semiarid environments during the middle Miocene to Pliocene. Ancestral state reconstruction of habitat indicates that the saxicolous habitat is apomorphic and independently evolved multiple times in Orthotrichum and Ulota, which supports the former hypothesis. Considering morphological statistics, the development of the cryptopore in Orthotrichum could provide increased resilience to dry habitats, and might promote their habitat shift during evolution.

    We reconstructed the phylogeny of two moss genera, Ulota and Orthotrichum, using three data matrices: (i) organellar genomes and 33 taxa; (ii) six molecular loci and 144 taxa; and (iii) two plastid loci and 163 taxa (not shown here). Our results, based on the maximum sampling of genes or taxa to date, generally confirm the new classification of the two genera and also provide some new findings, including all Ulota species except Ulota phyllantha forming a clade (Ulota I) and three lineages comprising the cryptoporous Orthotrichum clade (Orthotrichum II). We estimated the time of the origin of immersed stomata, and reconstructed the ancestral states of stomata and habitat. Our findings confirm the previous morphological based hypotheses about the evolution pathway of three types of stomata and further reveal that the occurrence of immersed stomata is probably related to arid environments, whereas the appearance of semi-immersed stomata could be associated with the mesic–xeric or semiarid environments. The cryptoporous feature of Orthotrichum perhaps helps them to be more resistant to dry habitats, that could promote their habitat shift from trees to rocks.
  • Bao Nie, Bo-Han Jiao, Li-Fei Ren, Polina D. Gudkova, Wen-Li Chen, and Wen-Hao Zhang
    J Syst Evol. 2022, 60(4): 901-913.
    https://doi.org/10.1111/jse.12714

    Stipa shanxiensis, a cryptic species within Stipa grandis that originated from central and western China, is described based on morphological, genomic, and ecological data from field and common garden experiments. Stipa shanxiensis morphologically resembles S. grandis, although phylogenetically it is closely related to the less morphologically similar Stipa baicalensis and Stipa krylovii. Of the eight significant morphological differences between S. shanxiensis and S. grandis, the two, cauline ligules longer than 2 cm with a filiform apex, and hairs shorter than 0.2 mm on the adaxial surface of the cauline uppermost leaves can be used to distinguish the species. Results from a common garden experiment verified that the two diagnostic characteristics were relatively stable and less morphologically plastic in response to environmental variation. Furthermore, a significant ecological divergence was found between S. shanxiensis and S. grandis, such that the former preferred warmer and more humid climates, and their predicted distribution was generally separated. Taken together, our results highlight that the integrative taxonomic approach was valuable for recognizing a new cryptic species in Stipa. In particular, we find that common garden experiments involving the effects of growth stage and characteristic position helped to morphologically diagnose cryptic species. These findings may also facilitate our understandings of ecological adaption and phenotypic plasticity in response to environmental change.

    We described a cryptic species Stipa shanxiensis within Stipa grandis, which originated from the central and western China, based on morphological, genomic, and ecological data from field and common garden experiments, highlighting that the integrative taxonomic approach was valuable for recognizing a new cryptic species in Stipa.
  • María J. Cano, Juan A. Jiménez, M. Teresa Gallego, and Juan Guerra
    J Syst Evol. 2022, 60(4): 914-931.
    https://doi.org/10.1111/jse.12801

    Pseudocrossidium is a genus of 21 species belonging to the Pottiaceae with the highest concentration of taxa and morphological variation found in South America. To investigate the evolutionary relationships among the species of Pseudocrossidium and other members of the Pottioideae, molecular phylogenetic reconstructions, using the nuclear ITS1-5.8S-ITS2, and the plastid atpB-rbcL, trnG, and trnL-F, has been performed because this genus has only been partially tested using molecular markers. Bayesian and maximum likelihood topologies show that the genus, as presently circumscribed, is polyphyletic. Consequently, the circumscription of Pseudocrossidium is amended and numerous taxonomic changes resulting from the molecular, morphological, and nomenclatural studies are proposed. The phylogenetic and morphologically divergent Pseudocrossidium mendozense is renamed as Gertrudiella mendozensis. Pseudocrossidium linearifolium and P. porphyreoneurum are representatives of the new genera Barbulastrum and Helicobarbula, respectively. Pseudocrossidium carinatum and P. santiagense are accommodated in a new genus Austrobarbula. Aloinella, nested in a paraphyletic Pseudocrossidium, is maintained at generic rank, apparently derived from Pseudocrossidium. Barbula integrifolia, B. riograndensis, and Tortula jaffuelii are transferred to Pseudocrossidium. The remaining species of Pseudocrossidium are maintained in this genus, pending further studies. Conflicts of the trees observed could be evidence of interspecific or intergeneric gene flow in various lineages in the Pottioideae.

    A molecular approach to the phylogeny of the moss genus Pseudocrossidium shows that, as presently circumscribed, the genus is polyphyletic. Our data suggest the description of three new genera to accommodate P. linearifolium, P. porphyreoneuron, and P. carinatum together with P. santiagense, respectively, and a new combination of Pseudocrossidium mendozense in Gertrudiella. In addition, new combinations are made for species previously included in Barbula and Tortula. The remaining Pseudocrossidium and Aloinella, despite its paraphyletic position, are provisionally maintained as separate genera.
  • Valentine Bouju, Kathrin Feldberg, Ulla Kaasalainen, Alfons Schäfer-Verwimp, Lars Hedenäs, William R. Buck, Bo Wang, Vincent Perrichot, and Alexander R. Schmidt
    J Syst Evol. 2022, 60(4): 932-954.
    https://doi.org/10.1111/jse.12796

    Amber is renowned for the exceptional preservation state of its inclusions, allowing detailed morphological analysis and providing relevant environmental, palaeoecological, geographical, and geological information. Amber deposits are predominantly known from North America, Europe, and Asia, and are considered to be rare on the continents that formed Gondwana. The recent discovery of fossiliferous amber deposits in Ethiopia, therefore, provides an inimitable opportunity to close gaps in the fossil record of African terrestrial biota and to study organisms which are otherwise rare in the fossil record. Here we show that diverse cryptogams are preserved in highest fidelity in Miocene Ethiopian amber. We describe gametophyte fragments of four liverworts: Thysananthus aethiopicus sp. nov. (Porellales, Lejeuneaceae), Lejeunea abyssinicoides sp. nov. (Porellales, Lejeuneaceae), Frullania shewanensis sp. nov. (Porellales, Frullaniaceae), and Frullania palaeoafricana sp. nov. (Porellales, Frullaniaceae). Furthermore, we describe a pleurocarpous moss of the extant genus Isopterygium (Hypnales, Pylaisiadelphaceae) and a lichen representing the order Lecanorales. These new specimens represent the first amber fossils of liverworts, mosses, and lichens from the African continent and render Ethiopian amber as one of the few worldwide amber deposits preserving bryophytes (mosses and liverworts) or lichens. Fossil species of Thysananthus were recorded in Eocene Baltic and Oligocene Bitterfeld as well as Miocene Dominican and probably also Miocene Mexican ambers. Fossils that can unequivocally be assigned to Lejeunea have only been found in Dominican amber so far. Neotropical ambers contain only one taxon of Frullania to date, while the genus is most diverse in Baltic, Bitterfeld, and Rovno ambers, formed in temperate regions. The new fossils support a tropical to subtropical origin of Ethiopian amber. The new African liverwort fossils are included in an updated list of leafy liverworts described from worldwide Cenozoic ambers to date.

    The first African amber fossils of liverworts, mosses, and lichens are reported from Miocene Ethiopian amber. The new fossils show an exceptional life-like preservation in crystal clear amber and four new species of liverworts are described. The cryptogam association, similar to that of Dominican amber, supports a tropical environment of Miocene Ethiopia.
  • Guang-Lin He, Meng-Ge Wang, Ying-Xiang Li, Xing Zou, Hui-Yuan Yeh, Ren-Kuan Tang, Xiao-Min Yang, Zheng Wang, Jian-Xin Guo, Ting Luo, Jing Zhao, Jin Sun, Rong Hu, Lan-Hai Wei, Gang Chen, Yi-Ping Hou, and Chuan-Chao Wang
    J Syst Evol. 2022, 60(4): 955-972.
    https://doi.org/10.1111/jse.12715

    The Han Chinese are the world's largest ethnic group residing across China. Shaanxi province in northern China was a pastoral–agricultural interlacing region sensitive to climate change since Neolithic times, which makes it a vital place for studying population dynamics. However, genetic studies of Shaanxi Han are underrepresented due to the lack of high-density sampling and genome-wide data. Here, we genotyped 700 000 single nucleotide polymorphisms (SNPs) in 200 Han individuals from nine populations in Shaanxi and compared with available modern and ancient Eurasian individuals. We revealed a north–south genetic cline in Han Chinese with Shaanxi Han locating at the northern side of the cline. We detected the western Eurasian-related admixture in Shaanxi populations, especially in Guanzhong and Shanbei Han Chinese in proportions of 2%–4.6%. Shaanxi Han were suggested to derive a large part of ancestry (39%–69%) from a lineage that also contributed largely to ancient and present-day Tibetans (85%) as well as southern Han, supporting the common northern China origin of modern Sino-Tibetan-speaking populations and southwestward expansion of millet farmers from the middle-upper Yellow River Basin to the Tibetan Plateau and to southern China. The rest of the ancestry of Shaanxi Han was from a lineage closely related to ancient and present-day Austronesian and Tai-Kadai speaking populations in southern China and Southeast Asia. We also observed a genetic substructure in Shaanxi Han in terms of north–south-related ancestry corresponding well to the latitudes. Maternal mitochondrial DNA and paternal Y-chromosome lineages further demonstrated the aforementioned admixture pattern of Han Chinese in Shaanxi province.

    The Han Chinese are the world's largest ethnic group residing across China. Shaanxi Province in northern China was a pastoral–agricultural interlacing region sensitive to climate change since Neolithic times, which makes it a vital place for studying population dynamics. However, genetic studies of Shaanxi Hans are underrepresented due to the lack of high-density sampling and genome-wide data. Here, we genotyped 700 000 single nucleotide polymorphisms (SNPs) in 200 Han individuals from nine populations in Shaanxi and compared with available modern and ancient Eurasian individuals. We revealed a north–south genetic cline in Han Chinese with Shaanxi Hans locating at the northern side of the cline. We detected the western Eurasian-related admixture in Shaanxi populations, especially in Guanzhong and Shanbei Han Chinese in proportions of 2%–4.6%. Shaanxi Hans were suggested to derive a large part of ancestry (39%–69%) from a lineage that also contributed largely to ancient and present-day Tibetans (85%) as well as southern Hans, supporting the common northern China origin of modern Sino-Tibetan-speaking populations and southwestward expansion of millet farmers from middle-upper Yellow River Basin to the Tibetan Plateau and to southern China. The rest of the ancestry of Shaanxi Hans was from a lineage closely related to ancient and present-day Austronesian and Tai-Kadai speaking populations in southern China and Southeast Asia. We also observed a genetic substructure in Shaanxi Hans in terms of north–south-related ancestry corresponding well to the latitudes. Maternal mitochondrial DNA and paternal Y-chromosome lineages further demonstrated the aforementioned admixture pattern of Han Chinese in Shaanxi Province.