Publications by authors named "Mark W Chase"

147 Publications

Plastid phylogenomics resolves ambiguous relationships within the orchid family and provides a solid timeframe for biogeography and macroevolution.

Sci Rep 2021 Mar 25;11(1):6858. Epub 2021 Mar 25.

Laboratorio de Biología Comparativa, Corporación Para Investigaciones Biológicas (CIB), Cra. 72 A No. 78 B 141, Medellín, Colombia.

Recent phylogenomic analyses based on the maternally inherited plastid organelle have enlightened evolutionary relationships between the subfamilies of Orchidaceae and most of the tribes. However, uncertainty remains within several subtribes and genera for which phylogenetic relationships have not ever been tested in a phylogenomic context. To address these knowledge-gaps, we here provide the most extensively sampled analysis of the orchid family to date, based on 78 plastid coding genes representing 264 species, 117 genera, 18 tribes and 28 subtribes. Divergence times are also provided as inferred from strict and relaxed molecular clocks and birth-death tree models. Our taxon sampling includes 51 newly sequenced plastid genomes produced by a genome skimming approach. We focus our sampling efforts on previously unplaced clades within tribes Cymbidieae and Epidendreae. Our results confirmed phylogenetic relationships in Orchidaceae as recovered in previous studies, most of which were recovered with maximum support (209 of the 262 tree branches). We provide for the first time a clear phylogenetic placement for Codonorchideae within subfamily Orchidoideae, and Podochilieae and Collabieae within subfamily Epidendroideae. We also identify relationships that have been persistently problematic across multiple studies, regardless of the different details of sampling and genomic datasets used for phylogenetic reconstructions. Our study provides an expanded, robust temporal phylogenomic framework of the Orchidaceae that paves the way for biogeographical and macroevolutionary studies.
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http://dx.doi.org/10.1038/s41598-021-83664-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7994851PMC
March 2021

Biogeography and genome size evolution of the oldest extant vascular plant genus, Equisetum (Equisetaceae).

Ann Bot 2021 Feb 18. Epub 2021 Feb 18.

Royal Botanic Gardens, Kew, Richmond, UK.

Background And Aims: Extant plant groups with a long fossil history are key elements in understanding vascular plant evolution. Horsetails (Equisetum, Equisetaceae) have a nearly continuous fossil record dating back to the Carboniferous, but their phylogenetic and biogeographic patterns are still poorly understood. We use here the most extensive phylogenetic analysis to date as a framework to evaluate their age, biogeography and genome size evolution.

Methods: DNA sequences of four plastid loci were used to estimate divergence times and investigate the biogeographic history of all extant species of Equisetum. Flow cytometry was used to study genome size evolution against the framework of phylogenetic relationships in Equisetum.

Key Results: On a well-supported phylogenetic tree including all extant Equisetum species, a molecular clock calibrated with multiple fossils places the node at which the outgroup and Equisetum diverged at 343 Mya (Early Carboniferous), with the first major split among extant species occurring 170 Mya (Middle Jurassic). These dates are older than those reported in some other recent molecular clock studies but are largely in agreement with a timeline established by fossil appearance in the geological record. Representatives of evergreen subgenus Hippochaete have much larger genome sizes than those of deciduous subgenus Equisetum, despite their shared conserved chromosome number. Subgenus Paramochaete has an intermediate genome size and maintains the same number of chromosomes.

Conclusions: The first divergences among extant members of the genus coincided with the break-up of Pangaea and the resulting more humid, warmer climate. Subsequent tectonic activity most likely involved vicariance events that led to species divergences combined with some more recent, long-distance dispersal events. We hypothesize that differences in genome size between subgenera may be related to the number of sperm flagellae.
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http://dx.doi.org/10.1093/aob/mcab005DOI Listing
February 2021

Diversification in Qinghai-Tibet Plateau: Orchidinae (Orchidaceae) clades exhibiting pre-adaptations play critical role.

Mol Phylogenet Evol 2021 04 31;157:107062. Epub 2020 Dec 31.

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 10093, China. Electronic address:

We explore the origins of the extraordinary plant diversity in the Qinghai-Tibetan Plateau (QTP) using Orchidinae (Orchidaceae) as a model. Our results indicate that six major clades in Orchidinae exhibited substantial variation in the temporal and spatial sequence of diversification. Our time-calibrated phylogenetic model suggests that the species-richness of Orchidinae arose through a combination of in situ diversification, colonisation, and local recruitment. There are multiple origins of species-richness of Orchidinae in the QTP, and pre-adaptations in clades from North Temperate and alpine regions were crucial for in situ diversification. The geographic analysis identified 29 dispersals from Asia, Africa and Europe into the QTP and 15 dispersals out. Most endemic species of Orchidinae evolved within the past six million years.
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http://dx.doi.org/10.1016/j.ympev.2020.107062DOI Listing
April 2021

Comparative Plastid Genomics of Neotropical (Orchidaceae; Epidendroideae).

Front Plant Sci 2020 3;11:799. Epub 2020 Jul 3.

Departamento de Botânica, Universidade Federal do Paraná, Curitiba, Brazil.

Pantropical , with ∼2,200 species, is one of the largest genera in Orchidaceae. Although phylogenetics and taxonomy of the ∼60 American species in the genus are generally well understood, some species complexes need more study to clearly delimit their component species and provide information about their evolutionary history. Previous research has suggested that the plastid genome includes phylogenetic markers capable of providing resolution at low taxonomic levels, and thus it could be an effective tool if these divergent regions can be identified. In this study, we sequenced the complete plastid genome of eight species, representing five of six Neotropical taxonomic sections. All plastomes conserve the typical quadripartite structure, and, although the general structure of plastid genomes is conserved, differences in -gene composition and total length were detected. Total length was determined by contraction and expansion of the small single-copy region, a result of an independent loss of the seven genes. Selection analyses indicated that protein-coding genes were generally well conserved, but in four genes, we identified 95 putative sites under positive selection. Furthermore, a total of 54 polymorphic simple sequence repeats were identified, for which we developed amplification primers. In addition, we propose 10 regions with potential to improve phylogenetic analyses of Neotropical species.
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http://dx.doi.org/10.3389/fpls.2020.00799DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7347972PMC
July 2020

Implications of plastome evolution in the true lilies (monocot order Liliales).

Mol Phylogenet Evol 2020 07 12;148:106818. Epub 2020 Apr 12.

Department of Life Science, Gachon University, Seongnam 13120, Republic of Korea. Electronic address:

The families of the monocot order Liliales exhibit highly contrasting characteristic of photosynthetic and mycoheterotrophic life histories. Although previous phylogenetic and morphological studies of Liliales have been conducted, they have not examined molecular evolution associated with this contrasting phenomenon. Here, we conduct the first comparative plastome study of all ten families of Liliales using 29 newly sequenced plastid genomes analyzed together with previously published data. We also present a phylogenetic analysis for Liliales of 78 plastid genes combined with 22 genes from all three genomes (nuclear 18S rDNA and phyC; 17 plastid genes; and mitochondrial matR, atpA, and cob). Within the newly generated phylogenetic tree of Liliales, we evaluate the ancestral state changes of selected morphological traits in the order. There are no significant differences in plastid genome features among species that show divergent characteristics correlated with family circumscriptions. However, the results clearly differentiate between photosynthetic and mycoheterotrophic taxa of Liliales in terms of genome structure, and gene content and order. The newly sequenced plastid genomes and combined three-genome data revealed Smilacaceae as sister to Liliaceae instead of Philesiaceae and Ripogonaceae. Additionally, we propose a revised familial classification system of Liliales that consists of nine families, considering Ripogonaceae a synonym of Philesiaceae. The ancestral state reconstruction indicated synapomorphies for each family of Liliales, except Liliaceae, Melanthiaceae and Colchicaceae. A taxonomic key for all nine families of Liliales is also provided.
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http://dx.doi.org/10.1016/j.ympev.2020.106818DOI Listing
July 2020

Repetitive DNA Restructuring Across Multiple Allopolyploidisation Events Shows a Lack of Strong Cytoplasmic Bias in Influencing Repeat Turnover.

Genes (Basel) 2020 02 19;11(2). Epub 2020 Feb 19.

School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, UK.

Allopolyploidy is acknowledged as an important force in plant evolution. Frequent allopolyploidy in across different timescales permits the evaluation of genome restructuring and repeat dynamics through time. Here we use a clustering approach on high-throughput sequence reads to identify the main classes of repetitive elements following three allotetraploid events, and how these are inherited from the closest extant relatives of the maternal and paternal subgenome donors. In all three cases, there was a lack of clear maternal, cytoplasmic bias in repeat evolution, i.e., lack of a predicted bias towards maternal subgenome-derived repeats, with roughly equal contributions from both parental subgenomes. Different overall repeat dynamics were found across timescales of <0.5 ( L.), 4 ( Willd.) and 6 ( Domin) Ma, with nearly additive, genome upsizing, and genome downsizing, respectively. Lower copy repeats were inherited in similar abundance to the parental subgenomes, whereas higher copy repeats contributed the most to genome size change in and . Genome downsizing post-polyploidisation may be a general long-term trend across angiosperms, but at more recent timescales there is species-specific variance as found in .
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http://dx.doi.org/10.3390/genes11020216DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7074350PMC
February 2020

Characterization of sequence variability hotspots in Cranichideae plastomes (Orchidaceae, Orchidoideae).

PLoS One 2020 28;15(1):e0227991. Epub 2020 Jan 28.

Royal Botanic Gardens, Kew, Richmond, Surrey, England, United Kingdom.

This study reports complete plastome sequences for six species of Neotropical Cranichideae and focuses on identification of the most variable regions (hotspots) in this group of orchids. These structure of these six plastomes is relatively conserved, exhibiting lengths ranging between 142,599 to 154,562 bp with 36.7% GC on average and exhibiting typical quadripartite arrangement (LSC, SSC and two IRs). Variation detected in the LSC/IR and SSC/IR junctions is explained by the loss of ndhF and ycf1 length variation. For the two genera of epiphytic clade in Spiranthinae, almost whole sets of the ndh-gene family were missing. Eight mutation hotspots were identified based on nucleotide diversity, sequence variability and parsimony-informative sites. Three of them (rps16-trnQ, trnT-trnL, rpl32-trnL) seem to be universal hotspots in the family, and the other five (trnG-trnR, trnR-atpA, trnP-psaJ, rpl32-infA, and rps15-ycf1) are described for the first time as orchid molecular hotspots. These regions have much more variation than all those used previously in phylogenetics of the group and offer useful plastid markers for phylogenetic, barcoding and population genetic studies. The use of whole plastomes or exclusive no-gap matrices also positioned with high support the holomycotrophic Rhizanthella among Orchidoideae plastomes in model-based analyses, showing the utility of plastomes for phylogenetic placement of this unusual genus.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0227991PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6986716PMC
April 2020

Plastome phylogenomics, biogeography, and clade diversification of Paris (Melanthiaceae).

BMC Plant Biol 2019 Dec 5;19(1):543. Epub 2019 Dec 5.

Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, Yunnan, China.

Background: Paris (Melanthiaceae) is an economically important but taxonomically difficult genus, which is unique in angiosperms because some species have extremely large nuclear genomes. Phylogenetic relationships within Paris have long been controversial. Based on complete plastomes and nuclear ribosomal DNA (nrDNA) sequences, this study aims to reconstruct a robust phylogenetic tree and explore historical biogeography and clade diversification in the genus.

Results: All 29 species currently recognized in Paris were sampled. Whole plastomes and nrDNA sequences were generated by the genome skimming approach. Phylogenetic relationships were reconstructed using the maximum likelihood and Bayesian inference methods. Based on the phylogenetic framework and molecular dating, biogeographic scenarios and historical diversification of Paris were explored. Significant conflicts between plastid and nuclear datasets were identified, and the plastome tree is highly congruent with past interpretations of the morphology. Ancestral area reconstruction indicated that Paris may have originated in northeastern Asia and northern China, and has experienced multiple dispersal and vicariance events during its diversification. The rate of clade diversification has sharply accelerated since the Miocene/Pliocene boundary.

Conclusions: Our results provide important insights for clarifying some of the long-standing taxonomic debates in Paris. Cytonuclear discordance may have been caused by ancient and recent hybridizations in the genus. The climatic and geological changes since the late Miocene, such as the intensification of Asian monsoon and the rapid uplift of Qinghai-Tibet Plateau, as well as the climatic fluctuations during the Pleistocene, played essential roles in driving range expansion and radiative diversification in Paris. Our findings challenge the theoretical prediction that large genome sizes may limit speciation.
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http://dx.doi.org/10.1186/s12870-019-2147-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6896732PMC
December 2019

Phylogenomics of Orchidaceae based on plastid and mitochondrial genomes.

Mol Phylogenet Evol 2019 10 25;139:106540. Epub 2019 Jun 25.

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, China; Southeast Asia Biodiversity Research Institute, Chinese Academy of Science (CAS-SEABRI), China. Electronic address:

To advance our knowledge of orchid relationships and timing of their relative divergence, we used 76 protein-coding genes from plastomes (ptCDS) and 38 protein-coding genes from mitochondrial genomes (mtCDS) of 74 orchids representing the five subfamilies and 18 tribes of Orchidaceae, to reconstruct the phylogeny and temporal evolution of the Orchidaceae. In our results, the backbone of orchid tree well supported with both datasets, but there are conflicts between these trees. The phylogenetic positions of two subfamilies (Vanilloideae and Cypripedioideae) are reversed in these two analyses. The phylogenetic positions of several tribes and subtribes, such as Epipogiinae, Gastrodieae, Nerviliinae, and Tropidieae, are well resolved in mtCDS tree. Thaieae have a different position among higher Epidendroideae, instead of sister to the higher Epidendroideae. Interrelationships of several recently radiated tribes within Epidendroideae, including Vandeae, Collabieae, Cymbidieae, Epidendreae, Podochileae, and Vandeae, have good support in the ptCDS tree, but most are not resolved in the mtCDS tree. Conflicts between the two datasets may be attributed to the different substitution rates in these two genomes and heterogeneity of substitution rate of plastome. Molecular dating indicated that the first three subfamilies, Apostasioideae, Cypripedioideae and Vanilloideae, diverged relatively quickly, and then there was a longer period before the last two subfamilies, Orchidoideae and Epidendroideae, began to radiate. Most mycoheterotrophic clades of Orchidaceae evolved in the last 30 million years with the exception of Gastrodieae.
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http://dx.doi.org/10.1016/j.ympev.2019.106540DOI Listing
October 2019

Phylogenomic Relationships of Diploids and the Origins of Allotetraploids in Dactylorhiza (Orchidaceae).

Syst Biol 2020 01;69(1):91-109

Department of Botany and Biodiversity Research, University of Vienna, Rennweg 14, A-1030 Vienna, Austria.

Disentangling phylogenetic relationships proves challenging for groups that have evolved recently, especially if there is ongoing reticulation. Although they are in most cases immediately isolated from diploid relatives, sets of sibling allopolyploids often hybridize with each other, thereby increasing the complexity of an already challenging situation. Dactylorhiza (Orchidaceae: Orchidinae) is a genus much affected by allopolyploid speciation and reticulate phylogenetic relationships. Here, we use genetic variation at tens of thousands of genomic positions to unravel the convoluted evolutionary history of Dactylorhiza. We first investigate circumscription and relationships of diploid species in the genus using coalescent and maximum likelihood methods, and then group 16 allotetraploids by maximum affiliation to their putative parental diploids, implementing a method based on genotype likelihoods. The direction of hybrid crosses is inferred for each allotetraploid using information from maternally inherited plastid RADseq loci. Starting from age estimates of parental taxa, the relative ages of these allotetraploid entities are inferred by quantifying their genetic similarity to the diploids and numbers of private alleles compared with sibling allotetraploids. Whereas northwestern Europe is dominated by young allotetraploids of postglacial origins, comparatively older allotetraploids are distributed further south, where climatic conditions remained relatively stable during the Pleistocene glaciations. Our bioinformatics approach should prove effective for the study of other naturally occurring, nonmodel, polyploid plant complexes.
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http://dx.doi.org/10.1093/sysbio/syz035DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6902629PMC
January 2020

Origin of angiosperms and the puzzle of the Jurassic gap.

Nat Plants 2019 05 6;5(5):461-470. Epub 2019 May 6.

Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, China.

Angiosperms are by far the most species-rich clade of land plants, but their origin and early evolutionary history remain poorly understood. We reconstructed angiosperm phylogeny based on 80 genes from 2,881 plastid genomes representing 85% of extant families and all orders. With a well-resolved plastid tree and 62 fossil calibrations, we dated the origin of the crown angiosperms to the Upper Triassic, with major angiosperm radiations occurring in the Jurassic and Lower Cretaceous. This estimated crown age is substantially earlier than that of unequivocal angiosperm fossils, and the difference is here termed the 'Jurassic angiosperm gap'. Our time-calibrated plastid phylogenomic tree provides a highly relevant framework for future comparative studies of flowering plant evolution.
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http://dx.doi.org/10.1038/s41477-019-0421-0DOI Listing
May 2019

Early consequences of allopolyploidy alter floral evolution in Nicotiana (Solanaceae).

BMC Plant Biol 2019 Apr 27;19(1):162. Epub 2019 Apr 27.

Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, 92521, USA.

Background: Polyploidy has played a major role in angiosperm evolution. Previous studies have examined polyploid phenotypes in comparison to their extant progenitors, but not in context of predicted progenitor phenotypes at allopolyploid origin. In addition, differences in the trends of polyploid versus diploid evolution have not been investigated. We use ancestral character-state reconstructions to estimate progenitor phenotype at allopolyploid origin to determine patterns of polyploid evolution leading to morphology of the extant species. We also compare trends in diploid versus allopolyploid evolution to determine if polyploidy modifies floral evolutionary patterns.

Results: Predicting the ancestral phenotype of a nascent allopolyploid from reconstructions of diploid phenotypes at the time of polyploid formation generates different phenotype predictions than when extant diploid phenotypes are used, the outcome of which can alter conclusions about polyploid evolution; however, most analyses yield the same results. Using ancestral reconstructions of diploid floral phenotypes indicate that young polyploids evolve shorter, wider corolla tubes, but older polyploids and diploids do not show any detectable evolutionary trends. Lability of the traits examined (floral shape, corolla tube length, and corolla tube width) differs across young and older polyploids and diploids. Corolla length is more evolutionarily labile in older polyploids and diploids. Polyploids do not display unique suites of floral characters based on both morphological and color traits, but some suites of characters may be evolving together and seem to have arisen multiple times within Nicotiana, perhaps due to the influence of pollinators.

Conclusions: Young polyploids display different trends in floral evolution (shorter, wider corolla tubes, which may result in more generalist pollination) than older polyploids and diploids, suggesting that patterns of divergence are impacted by the early consequences of allopolyploidy, perhaps arising from genomic shock and/or subsequent genome stabilization associated with diploidization. Convergent evolution in floral morphology and color in Nicotiana can be consistent with pollinator preferences, suggesting that pollinators may have shaped floral evolution in Nicotiana.
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http://dx.doi.org/10.1186/s12870-019-1771-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6486959PMC
April 2019

Plastid phylogenomic insights into the evolution of Caryophyllales.

Mol Phylogenet Evol 2019 05 5;134:74-86. Epub 2019 Feb 5.

Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China; Key Laboratory for Plant Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China. Electronic address:

The Caryophyllales includes 40 families and 12,500 species, representing a large and diverse clade of angiosperms. Collectively, members of the clade grow on all continents and in all terrestrial biomes and often occupy extreme habitats (e.g., xeric, salty). The order is characterized by many taxa with unusual adaptations including carnivory, halophytism, and multiple origins of C photosynthesis. However, deep phylogenetic relationships within the order have long been problematic due to putative rapid divergence. To resolve the deep-level relationships of Caryophyllales, we performed phylogenomic analyses of all 40 families of Caryophyllales. We time-calibrated the molecular phylogeny of this clade, and evaluated putative correlations among plastid structural changes and rates of molecular substitution. We recovered a well-resolved and well-supported phylogeny of the Caryophyllales that was largely congruent with previous estimates of this order. Our results provide improved support for the phylogenetic position of several key families within this clade. The crown age of Caryophyllales was estimated at ca. 114.4 million years ago (Ma), with periods of rapid divergence in the mid-Cretaceous. A strong, positive correlation between nucleotide substitution rate and plastid structural changes was detected. Our study highlights the importance of broad taxon sampling in phylogenomic inference and provides a firm basis for future investigations of molecular, morphological, and ecophysiological evolution in Caryophyllales.
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http://dx.doi.org/10.1016/j.ympev.2018.12.023DOI Listing
May 2019

Molecular phylogenomics of the tribe Shoreeae (Dipterocarpaceae) using whole plastid genomes.

Ann Bot 2019 05;123(5):857-865

University of Vienna, Department of Botany and Biodiversity Research, Rennweg, Vienna, Austria.

Background And Aims: Phylogenetic relationships within tribe Shoreeae, containing the main elements of tropical forests in Southeast Asia, present a long-standing problem in the systematics of Dipterocarpaceae. Sequencing whole plastomes using next-generation sequencing- (NGS) based genome skimming is increasingly employed for investigating phylogenetic relationships of plants. Here, the usefulness of complete plastid genome sequences in resolving phylogenetic relationships within Shoreeae is evaluated.

Methods: A pipeline to obtain alignments of whole plastid genome sequences across individuals with different amounts of available data is presented. In total, 48 individuals, representing 37 species and four genera of the ecologically and economically important tribe Shoreeae sensu Ashton, were investigated. Phylogenetic trees were reconstructed using maximum parsimony, maximum likelihood and Bayesian inference.

Key Results: Here, the first fully sequenced plastid genomes for the tribe Shoreeae are presented. Their size, GC content and gene order are comparable with those of other members of Malvales. Phylogenomic analyses demonstrate that whole plastid genomes are useful for inferring phylogenetic relationships among genera and groups of Shorea (Shoreeae) but fail to provide well-supported phylogenetic relationships among some of the most closely related species. Discordance in placement of Parashorea was observed between phylogenetic trees obtained from plastome analyses and those obtained from nuclear single nucleotide polymorphism (SNP) data sets identified in restriction-site associated sequencing (RADseq).

Conclusions: Phylogenomic analyses of the entire plastid genomes are useful for inferring phylogenetic relationships at lower taxonomic levels, but are not sufficient for detailed phylogenetic reconstructions of closely related species groups in Shoreeae. Discordance in placement of Parashorea was further investigated for evidence of ancient hybridization.
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http://dx.doi.org/10.1093/aob/mcy220DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526321PMC
May 2019

Phylogenetics of subtribe Orchidinae s.l. (Orchidaceae; Orchidoideae) based on seven markers (plastid matK, psaB, rbcL, trnL-F, trnH-psba, and nuclear nrITS, Xdh): implications for generic delimitation.

BMC Plant Biol 2017 Nov 25;17(1):222. Epub 2017 Nov 25.

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 10093, China.

Background: Subtribe Orchidinae (Orchidaceae, Orchidoideae) are a nearly cosmopolitan taxon of terrestrial orchids, comprising about 1800 species in 47 to 60 genera. Although much progress has been made in recent years of phylogenetics of Orchidinae, considerable problems remain to be addressed. Based on molecular phylogenetics, we attempt to illustrate the phylogenetic relationships and discuss generic delimitation within Orchidinae. Seven DNA markers (five plastid and two nuclear), a broad sampling of Orchidinae (400 species in 52 genera) and three methods of phylogenetic analysis (maximum likelihood, maximum parsimony and Bayesian inference) were used.

Results: Orchidinae s.l. are monophyletic. Satyrium is sister to the rest of Orchidinae s.l. Brachycorythis and Schizochilus are successive sister to Asian-European Orchidinae s.s. Sirindhornia and Shizhenia are successive sister to clade formed by Tsaiorchis-Hemipilia-Ponerorchis alliance. Stenoglottis is sister to the Habenaria-Herminium-Peristylus alliance. Habenaria, currently the largest genus in Orchidinae, is polyphyletic and split into two distant clades: one Asian-Australian and the other African-American-Asian. Diplomeris is sister to Herminium s.l. plus Asian-Australian Habenaria.

Conclusions: We propose to recognize five genera in the Ponerorchis alliance: Hemipilia, Ponerorchis s.l., Sirindhornia, Shizhenia and Tsaiorchis. Splitting Habenaria into two genera based on morphological characters and geographical distribution may be the least disruptive approach, and it is reasonable to keep Satyrium in Orchidinae.
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http://dx.doi.org/10.1186/s12870-017-1160-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5702240PMC
November 2017

Independent degradation in genes of the plastid ndh gene family in species of the orchid genus Cymbidium (Orchidaceae; Epidendroideae).

PLoS One 2017 15;12(11):e0187318. Epub 2017 Nov 15.

Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey, United Kingdom.

In this paper, we compare ndh genes in the plastid genome of many Cymbidium species and three closely related taxa in Orchidaceae looking for evidence of ndh gene degradation. Among the 11 ndh genes, there were frequently large deletions in directly repeated or AT-rich regions. Variation in these degraded ndh genes occurs between individual plants, apparently at population levels in these Cymbidium species. It is likely that ndh gene transfers from the plastome to mitochondrial genome (chondriome) occurred independently in Orchidaceae and that ndh genes in the chondriome were also relatively recently transferred between distantly related species in Orchidaceae. Four variants of the ycf1-rpl32 region, which normally includes the ndhF genes in the plastome, were identified, and some Cymbidium species contained at least two copies of that region in their organellar genomes. The four ycf1-rpl32 variants seem to have a clear pattern of close relationships. Patterns of ndh degradation between closely related taxa and translocation of ndh genes to the chondriome in Cymbidium suggest that there have been multiple bidirectional intracellular gene transfers between two organellar genomes, which have produced different levels of ndh gene degradation among even closely related species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0187318PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5695243PMC
December 2017

Plant DNA barcodes and assessment of phylogenetic community structure of a tropical mixed dipterocarp forest in Brunei Darussalam (Borneo).

PLoS One 2017 19;12(10):e0185861. Epub 2017 Oct 19.

Department of Botany and Biodiversity Research, Faculty of Life Sciences, University of Vienna, Vienna, Austria.

DNA barcoding is a fast and reliable tool to assess and monitor biodiversity and, via community phylogenetics, to investigate ecological and evolutionary processes that may be responsible for the community structure of forests. In this study, DNA barcodes for the two widely used plastid coding regions rbcL and matK are used to contribute to identification of morphologically undetermined individuals, as well as to investigate phylogenetic structure of tree communities in 70 subplots (10 × 10m) of a 25-ha forest-dynamics plot in Brunei (Borneo, Southeast Asia). The combined matrix (rbcL + matK) comprised 555 haplotypes (from ≥154 genera, 68 families and 25 orders sensu APG, Angiosperm Phylogeny Group, 2016), making a substantial contribution to tree barcode sequences from Southeast Asia. Barcode sequences were used to reconstruct phylogenetic relationships using maximum likelihood, both with and without constraining the topology of taxonomic orders to match that proposed by the Angiosperm Phylogeny Group. A third phylogenetic tree was reconstructed using the program Phylomatic to investigate the influence of phylogenetic resolution on results. Detection of non-random patterns of community assembly was determined by net relatedness index (NRI) and nearest taxon index (NTI). In most cases, community assembly was either random or phylogenetically clustered, which likely indicates the importance to community structure of habitat filtering based on phylogenetically correlated traits in determining community structure. Different phylogenetic trees gave similar overall results, but the Phylomatic tree produced greater variation across plots for NRI and NTI values, presumably due to noise introduced by using an unresolved phylogenetic tree. Our results suggest that using a DNA barcode tree has benefits over the traditionally used Phylomatic approach by increasing precision and accuracy and allowing the incorporation of taxonomically unidentified individuals into analyses.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0185861PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5648112PMC
November 2017

Adaptive sequence evolution is driven by biotic stress in a pair of orchid species (Dactylorhiza) with distinct ecological optima.

Mol Ecol 2017 Jul 27;26(14):3649-3662. Epub 2017 Apr 27.

Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria.

The orchid family is the largest in the angiosperms, but little is known about the molecular basis of the significant variation they exhibit. We investigate here the transcriptomic divergence between two European terrestrial orchids, Dactylorhiza incarnata and Dactylorhiza fuchsii, and integrate these results in the context of their distinct ecologies that we also document. Clear signals of lineage-specific adaptive evolution of protein-coding sequences are identified, notably targeting elements of biotic defence, including both physical and chemical adaptations in the context of divergent pools of pathogens and herbivores. In turn, a substantial regulatory divergence between the two species appears linked to adaptation/acclimation to abiotic conditions. Several of the pathways affected by differential expression are also targeted by deviating post-transcriptional regulation via sRNAs. Finally, D. incarnata appears to suffer from insufficient sRNA control over the activity of RNA-dependent DNA polymerase, resulting in increased activity of class I transposable elements and, over time, in larger genome size than that of D. fuchsii. The extensive molecular divergence between the two species suggests significant genomic and transcriptomic shock in their hybrids and offers insights into the difficulty of coexistence at the homoploid level. Altogether, biological response to selection, accumulated during the history of these orchids, appears governed by their microenvironmental context, in which biotic and abiotic pressures act synergistically to shape transcriptome structure, expression and regulation.
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http://dx.doi.org/10.1111/mec.14123DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5518283PMC
July 2017

Diversification of Rosaceae since the Late Cretaceous based on plastid phylogenomics.

New Phytol 2017 May 10;214(3):1355-1367. Epub 2017 Feb 10.

Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, 650201, China.

Phylogenetic relationships in Rosaceae have long been problematic because of frequent hybridisation, apomixis and presumed rapid radiation, and their historical diversification has not been clarified. With 87 genera representing all subfamilies and tribes of Rosaceae and six of the other eight families of Rosales (outgroups), we analysed 130 newly sequenced plastomes together with 12 from GenBank in an attempt to reconstruct deep relationships and reveal temporal diversification of this family. Our results highlight the importance of improving sequence alignment and the use of appropriate substitution models in plastid phylogenomics. Three subfamilies and 16 tribes (as previously delimited) were strongly supported as monophyletic, and their relationships were fully resolved and strongly supported at most nodes. Rosaceae were estimated to have originated during the Late Cretaceous with evidence for rapid diversification events during several geological periods. The major lineages rapidly diversified in warm and wet habits during the Late Cretaceous, and the rapid diversification of genera from the early Oligocene onwards occurred in colder and drier environments. Plastid phylogenomics offers new and important insights into deep phylogenetic relationships and the diversification history of Rosaceae. The robust phylogenetic backbone and time estimates we provide establish a framework for future comparative studies on rosaceous evolution.
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http://dx.doi.org/10.1111/nph.14461DOI Listing
May 2017

Genome-wide repeat dynamics reflect phylogenetic distance in closely related allotetraploid (Solanaceae).

Plant Syst Evol 2017 1;303(8):1013-1020. Epub 2016 Nov 1.

1School of Biological and Chemical Sciences, Queen Mary University of London, London, E1 4NS UK.

sect. is a group of four allotetraploid species originating from a single allopolyploidisation event approximately 5 million years ago. Previous phylogenetic analyses support the hypothesis of as sister to the other three species. This is concordant with changes in genome size, separating those with genome downsizing () from those with genome upsizing (, , ). However, a recent analysis reflecting genome dynamics of different transposable element families reconstructed greater similarity between and the Revillagigedo Island taxa ( and ), thereby placing as sister to the rest of the group. This could reflect a different phylogenetic hypothesis or the unique evolutionary history of these particular elements. Here we re-examine relationships in this group and investigate genome-wide patterns in repetitive DNA, utilising high-throughput sequencing and a genome skimming approach. Repetitive DNA clusters provide support for as sister to the rest of the section, with sister to the two Revillagigedo Island species. Clade-specific patterns in the occurrence and abundance of particular repeats confirm the original ( ( ( + ))) hypothesis. Furthermore, overall repeat dynamics in the island species and confirm their similarity to and the distinctive patterns between these three species and . Together these results suggest that broad-scale repeat dynamics do in fact reflect evolutionary history and could be predicted based on phylogenetic distance.
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http://dx.doi.org/10.1007/s00606-016-1356-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6961477PMC
November 2016

Transgressive phenotypes and generalist pollination in the floral evolution of Nicotiana polyploids.

Nat Plants 2016 08 8;2:16119. Epub 2016 Aug 8.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK.

Polyploidy is an important driving force in angiosperm evolution, and much research has focused on genetic, epigenetic and transcriptomic responses to allopolyploidy. Nicotiana is an excellent system in which to study allopolyploidy because half of the species are allotetraploids of different ages, allowing us to examine the trajectory of floral evolution over time. Here, we study the effects of allopolyploidy on floral morphology in Nicotiana, using corolla tube measurements and geometric morphometrics to quantify petal shape. We show that polyploid morphological divergence from the intermediate phenotype expected (based on progenitor morphology) increases with time for floral limb shape and tube length, and that most polyploids are distinct or transgressive in at least one trait. In addition, we show that polyploids tend to evolve shorter and wider corolla tubes, suggesting that allopolyploidy could provide an escape from specialist pollination via reversion to more generalist pollination strategies.
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http://dx.doi.org/10.1038/nplants.2016.119DOI Listing
August 2016

Sequencing of whole plastid genomes and nuclear ribosomal DNA of Diospyros species (Ebenaceae) endemic to New Caledonia: many species, little divergence.

Ann Bot 2016 06 20;117(7):1175-85. Epub 2016 Apr 20.

Department of Botany and Biodiversity Research, Faculty of Life Sciences, University of Vienna, Rennweg 14, 1030 Wien, Austria.

Background And Aims: Some plant groups, especially on islands, have been shaped by strong ancestral bottlenecks and rapid, recent radiation of phenotypic characters. Single molecular markers are often not informative enough for phylogenetic reconstruction in such plant groups. Whole plastid genomes and nuclear ribosomal DNA (nrDNA) are viewed by many researchers as sources of information for phylogenetic reconstruction of groups in which expected levels of divergence in standard markers are low. Here we evaluate the usefulness of these data types to resolve phylogenetic relationships among closely related Diospyros species.

Methods: Twenty-two closely related Diospyros species from New Caledonia were investigated using whole plastid genomes and nrDNA data from low-coverage next-generation sequencing (NGS). Phylogenetic trees were inferred using maximum parsimony, maximum likelihood and Bayesian inference on separate plastid and nrDNA and combined matrices.

Key Results: The plastid and nrDNA sequences were, singly and together, unable to provide well supported phylogenetic relationships among the closely related New Caledonian Diospyros species. In the nrDNA, a 6-fold greater percentage of parsimony-informative characters compared with plastid DNA was found, but the total number of informative sites was greater for the much larger plastid DNA genomes. Combining the plastid and nuclear data improved resolution. Plastid results showed a trend towards geographical clustering of accessions rather than following taxonomic species.

Conclusions: In plant groups in which multiple plastid markers are not sufficiently informative, an investigation at the level of the entire plastid genome may also not be sufficient for detailed phylogenetic reconstruction. Sequencing of complete plastid genomes and nrDNA repeats seems to clarify some relationships among the New Caledonian Diospyros species, but the higher percentage of parsimony-informative characters in nrDNA compared with plastid DNA did not help to resolve the phylogenetic tree because the total number of variable sites was much lower than in the entire plastid genome. The geographical clustering of the individuals against a background of overall low sequence divergence could indicate transfer of plastid genomes due to hybridization and introgression following secondary contact.
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http://dx.doi.org/10.1093/aob/mcw060DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4904177PMC
June 2016

Processes Driving the Adaptive Radiation of a Tropical Tree (Diospyros, Ebenaceae) in New Caledonia, a Biodiversity Hotspot.

Syst Biol 2016 Mar 1;65(2):212-27. Epub 2015 Oct 1.

Department of Botany and Biodiversity Research, University of Vienna, 1030 Vienna, Austria;

Due to its special geological history, the New Caledonian Archipelago is a mosaic of soil types, and in combination with climatic conditions this results in a heterogeneous environment across relatively small distances. A group of over 20 endemic species of Diospyros (Ebenaceae) has rapidly and recently radiated on the archipelago after a single long-distance dispersal event. Most of the Diospyros species in the radiating group are morphologically and ecologically well differentiated, but they exhibit low levels of DNA variability. To investigate the processes that shaped the diversification of this group we employed restriction site associated DNA sequencing (RADseq). Over 8400 filtered SNPs generally confirm species delimitations and produce a well-supported phylogenetic tree. Our analyses document local introgression, but only a limited potential for gene flow over longer distances. The phylogenetic relationships point to an early regional clustering among populations and species, indicating that allopatric speciation with respect to macrohabitat (i.e., climatic conditions) may have had a role in the initial differentiation within the group. A later, more rapid radiation involved divergence with respect to microhabitat (i.e., soil preference). Several sister species in the group show a parallel divergence in edaphic preference. Searches for genomic regions that are systematically differentiated in this replicated phenotypic divergence pointed to loci potentially involved in ion binding and cellular transport. These loci appear meaningful in the context of adaptations to soil types that differ in heavy-metal and mineral content. Identical nucleotide changes affected only two of these loci, indicating that introgression may have played a limited role in their evolution. Our results suggest that both allopatric diversification and (parapatric) ecological divergence shaped successive rounds of speciation in the Diospyros radiation on New Caledonia.
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http://dx.doi.org/10.1093/sysbio/syv076DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4748748PMC
March 2016

Beyond the EDGE with EDAM: Prioritising British Plant Species According to Evolutionary Distinctiveness, and Accuracy and Magnitude of Decline.

PLoS One 2015 27;10(5):e0126524. Epub 2015 May 27.

Department of Life Sciences, Imperial College London, Ascot, Berkshire, United Kingdom; Centre for Ecology and Hydrology, Wallingford, Oxfordshire, United Kingdom; Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK.

Conservation biologists have only finite resources, and so must prioritise some species over others. The EDGE-listing approach ranks species according to their combined evolutionary distinctiveness and degree of threat, but ignores the uncertainty surrounding both threat and evolutionary distinctiveness. We develop a new family of measures for species, which we name EDAM, that incorporates evolutionary distinctiveness, the magnitude of decline, and the accuracy with which decline can be predicted. Further, we show how the method can be extended to explore phyogenetic uncertainty. Using the vascular plants of Britain as a case study, we find that the various EDAM measures emphasise different species and parts of Britain, and that phylogenetic uncertainty can strongly affect the prioritisation scores of some species.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0126524PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4446313PMC
April 2016

The effect of polyploidy and hybridization on the evolution of floral colour in Nicotiana (Solanaceae).

Ann Bot 2015 Jun 15;115(7):1117-31. Epub 2015 May 15.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK, Natural History Museum, London SW7 5BD, UK, Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK, Max Planck Institute for Chemical Ecology, Department of Molecular Ecology, Beutenberg Campus, Hans-Knöll-Strasse 8, 07745 Jena, Germany, Institute of Biophysics, Academy of Sciences of the Czech Republic, CZ-61265 Brno, Czech Republic, Institut Jean-Pierre Bourgin, UMR1318 INRA-AgroParisTech, INRA-Versailles, 78026 Versailles cedex, France and Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK

Background And Aims: Speciation in angiosperms can be accompanied by changes in floral colour that may influence pollinator preference and reproductive isolation. This study investigates whether changes in floral colour can accompany polyploid and homoploid hybridization, important processes in angiosperm evolution.

Methods: Spectral reflectance of corolla tissue was examined for 60 Nicotiana (Solanaceae) accessions (41 taxa) based on spectral shape (corresponding to pigmentation) as well as bee and hummingbird colour perception in order to assess patterns of floral colour evolution. Polyploid and homoploid hybrid spectra were compared with those of their progenitors to evaluate whether hybridization has resulted in floral colour shifts.

Key Results: Floral colour categories in Nicotiana seem to have arisen multiple times independently during the evolution of the genus. Most younger polyploids displayed an unexpected floral colour, considering those of their progenitors, in the colour perception of at least one pollinator type, whereas older polyploids tended to resemble one or both of their progenitors.

Conclusions: Floral colour evolution in Nicotiana is weakly constrained by phylogeny, and colour shifts do occur in association with both polyploid and homoploid hybrid divergence. Transgressive floral colour in N. tabacum has arisen by inheritance of anthocyanin pigmentation from its paternal progenitor while having a plastid phenotype like its maternal progenitor. Potentially, floral colour evolution has been driven by, or resulted in, pollinator shifts. However, those polyploids that are not sympatric (on a regional scale) with their progenitor lineages are typically not divergent in floral colour from them, perhaps because of a lack of competition for pollinators.
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http://dx.doi.org/10.1093/aob/mcv048DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4598364PMC
June 2015

Phylogenetic relationships in Epidendroideae (Orchidaceae), one of the great flowering plant radiations: progressive specialization and diversification.

Ann Bot 2015 Mar 11;115(4):665-81. Epub 2015 Jan 11.

Herbarium, Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, OH 43212, USA, Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond, Surrey TW9 3AE, UK and School of Plant Biology, The University of Western Australia, Crawley, WA 600, Australia Herbarium, Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, OH 43212, USA, Jodrell Laboratory, Royal Botanic Gardens Kew, Richmond, Surrey TW9 3AE, UK and School of Plant Biology, The University of Western Australia, Crawley, WA 600, Australia.

Background And Aims: The largest subfamily of orchids, Epidendroideae, represents one of the most significant diversifications among flowering plants in terms of pollination strategy, vegetative adaptation and number of species. Although many groups in the subfamily have been resolved, significant relationships in the tree remain unclear, limiting conclusions about diversification and creating uncertainty in the classification. This study brings together DNA sequences from nuclear, plastid and mitochrondrial genomes in order to clarify relationships, to test associations of key characters with diversification and to improve the classification.

Methods: Sequences from seven loci were concatenated in a supermatrix analysis for 312 genera representing most of epidendroid diversity. Maximum-likelihood and parsimony analyses were performed on this matrix and on subsets of the data to generate trees and to investigate the effect of missing values. Statistical character-associated diversification analyses were performed.

Key Results: Likelihood and parsimony analyses yielded highly resolved trees that are in strong agreement and show significant support for many key clades. Many previously proposed relationships among tribes and subtribes are supported, and some new relationships are revealed. Analyses of subsets of the data suggest that the relatively high number of missing data for the full analysis is not problematic. Diversification analyses show that epiphytism is most strongly associated with diversification among epidendroids, followed by expansion into the New World and anther characters that are involved with pollinator specificity, namely early anther inflexion, cellular pollinium stalks and the superposed pollinium arrangement.

Conclusions: All tested characters show significant association with speciation in Epidendroideae, suggesting that no single character accounts for the success of this group. Rather, it appears that a succession of key features appeared that have contributed to diversification, sometimes in parallel.
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http://dx.doi.org/10.1093/aob/mcu253DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4343289PMC
March 2015

Phylogeny, extinction and conservation: embracing uncertainties in a time of urgency.

Philos Trans R Soc Lond B Biol Sci 2015 Feb;370(1662):20140002

The Australian Museum, College Street, Sydney, New South Wales 2010, Australia.

Evolutionary studies have played a fundamental role in our understanding of life, but until recently, they had only a relatively modest involvement in addressing conservation issues. The main goal of the present discussion meeting issue is to offer a platform to present the available methods allowing the integration of phylogenetic and extinction risk data in conservation planning. Here, we identify the main knowledge gaps in biodiversity science, which include incomplete sampling, reconstruction biases in phylogenetic analyses, partly known species distribution ranges, and the difficulty in producing conservation assessments for all known species, not to mention that much of the effective biological diversity remains to be discovered. Given the impact that human activities have on biodiversity and the urgency with which we need to address these issues, imperfect assumptions need to be sanctioned and surrogates used in the race to salvage as much as possible of our natural and evolutionary heritage. We discuss some aspects of the uncertainties found in biodiversity science, such as the ideal surrogates for biodiversity, the gaps in our knowledge and the numerous available phylogenetic diversity-based methods. We also introduce a series of cases studies that demonstrate how evolutionary biology can effectively contribute to biodiversity conservation science.
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http://dx.doi.org/10.1098/rstb.2014.0002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4290416PMC
February 2015

Genomic repeat abundances contain phylogenetic signal.

Syst Biol 2015 Jan 25;64(1):112-26. Epub 2014 Sep 25.

School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK; Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK; School of Plant Biology, The University of Western Australia, Crawley WA 6009, Australia; Institute of Plant Molecular Biology, Biology Centre ASCR, Branišovská 31, České Budějovice, CZ-37005, Czech Republic; Systematic Botany and Mycology, University of Munich (LMU), Menzinger Straße 67, 80638 München, Germany; and Department of Systematic and Evolutionary Botany, University of Vienna, Rennweg 14, A-1030 Vienna, Austria

A large proportion of genomic information, particularly repetitive elements, is usually ignored when researchers are using next-generation sequencing. Here we demonstrate the usefulness of this repetitive fraction in phylogenetic analyses, utilizing comparative graph-based clustering of next-generation sequence reads, which results in abundance estimates of different classes of genomic repeats. Phylogenetic trees are then inferred based on the genome-wide abundance of different repeat types treated as continuously varying characters; such repeats are scattered across chromosomes and in angiosperms can constitute a majority of nuclear genomic DNA. In six diverse examples, five angiosperms and one insect, this method provides generally well-supported relationships at interspecific and intergeneric levels that agree with results from more standard phylogenetic analyses of commonly used markers. We propose that this methodology may prove especially useful in groups where there is little genetic differentiation in standard phylogenetic markers. At the same time as providing data for phylogenetic inference, this method additionally yields a wealth of data for comparative studies of genome evolution.
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http://dx.doi.org/10.1093/sysbio/syu080DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4265144PMC
January 2015

Trends and concepts in fern classification.

Ann Bot 2014 Mar 13;113(4):571-94. Epub 2014 Feb 13.

Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond TW9 3DS, UK.

Background And Aims: Throughout the history of fern classification, familial and generic concepts have been highly labile. Many classifications and evolutionary schemes have been proposed during the last two centuries, reflecting different interpretations of the available evidence. Knowledge of fern structure and life histories has increased through time, providing more evidence on which to base ideas of possible relationships, and classification has changed accordingly. This paper reviews previous classifications of ferns and presents ideas on how to achieve a more stable consensus.

Scope: An historical overview is provided from the first to the most recent fern classifications, from which conclusions are drawn on past changes and future trends. The problematic concept of family in ferns is discussed, with a particular focus on how this has changed over time. The history of molecular studies and the most recent findings are also presented.

Key Results: Fern classification generally shows a trend from highly artificial, based on an interpretation of a few extrinsic characters, via natural classifications derived from a multitude of intrinsic characters, towards more evolutionary circumscriptions of groups that do not in general align well with the distribution of these previously used characters. It also shows a progression from a few broad family concepts to systems that recognized many more narrowly and highly controversially circumscribed families; currently, the number of families recognized is stabilizing somewhere between these extremes. Placement of many genera was uncertain until the arrival of molecular phylogenetics, which has rapidly been improving our understanding of fern relationships. As a collective category, the so-called 'fern allies' (e.g. Lycopodiales, Psilotaceae, Equisetaceae) were unsurprisingly found to be polyphyletic, and the term should be abandoned. Lycopodiaceae, Selaginellaceae and Isoëtaceae form a clade (the lycopods) that is sister to all other vascular plants, whereas the whisk ferns (Psilotaceae), often included in the lycopods or believed to be associated with the first vascular plants, are sister to Ophioglossaceae and thus belong to the fern clade. The horsetails (Equisetaceae) are also members of the fern clade (sometimes inappropriately called 'monilophytes'), but, within that clade, their placement is still uncertain. Leptosporangiate ferns are better understood, although deep relationships within this group are still unresolved. Earlier, almost all leptosporangiate ferns were placed in a single family (Polypodiaceae or Dennstaedtiaceae), but these families have been redefined to narrower more natural entities.

Conclusions: Concluding this paper, a classification is presented based on our current understanding of relationships of fern and lycopod clades. Major changes in our understanding of these families are highlighted, illustrating issues of classification in relation to convergent evolution and false homologies. Problems with the current classification and groups that still need study are pointed out. A summary phylogenetic tree is also presented. A new classification in which Aspleniaceae, Cyatheaceae, Polypodiaceae and Schizaeaceae are expanded in comparison with the most recent classifications is presented, which is a modification of those proposed by Smith et al. (2006, 2008) and Christenhusz et al. (2011). These classifications are now finding a wider acceptance and use, and even though a few amendments are made based on recently published results from molecular analyses, we have aimed for a stable family and generic classification of ferns.
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http://dx.doi.org/10.1093/aob/mct299DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3936591PMC
March 2014