Qiu-Yun Jenny Xiang

Estimating ancestral distributions of lineages with uncertain sister groups: a statistical approach to Dispersal-Vicariance Analysis and a case using Aesculus L. (Sapindaceae) including fossils.

Abstract  We propose a simple statistical approach for using Dispersal–Vicariance Analysis (DIVA) software to infer biogeographic histories without fully bifurcating trees. In this approach, ancestral ranges are first optimized for a sample of Bayesian trees. The probability P of an ancestral range r at a node is then calculated as where Y is a node, and F(rY) is the frequency of range r among all the optimal solutions resulting from DIVA optimization at node Y, t is one of n topologies optimized, and Pt is the probability of topology t. Node Y is a hypothesized ancestor shared by a specific crown lineage and the sister of that lineage “x”, where x may vary due to phylogenetic uncertainty (polytomies and nodes with posterior probability <100%). Using this method, the ancestral distribution at Y can be estimated to provide inference of the geographic origins of the specific crown group of interest. This approach takes into account phylogenetic uncertainty as well as uncertainty from DIVA optimization. It is an extension of the previously described method called Bayes‐DIVA, which pairs Bayesian phylogenetic analysis with biogeographic analysis using DIVA. Further, we show that the probability P of an ancestral range at Y calculated using this method does not equate to pp*F(rY) on the Bayesian consensus tree when both variables are <100%, where pp is the posterior probability and F(rY) is the frequency of range r for the node containing the specific crown group. We tested our DIVA‐Bayes approach using Aesculus L., which has major lineages unresolved as a polytomy. We inferred the most probable geographic origins of the five traditional sections of Aesculus and of Aesculus californica Nutt. and examined range subdivisions at parental nodes of these lineages. Additionally, we used the DIVA‐Bayes data from Aesculus to quantify the effects on biogeographic inference of including two wildcard fossil taxa in phylogenetic analysis. Our analysis resolved the geographic ranges of the parental nodes of the lineages of Aesculus with moderate to high probabilities. The probabilities were greater than those estimated using the simple calculation of pp*F(ry) at a statistically significant level for two of the six lineages. We also found that adding fossil wildcard taxa in phylogenetic analysis generally increased P for ancestral ranges including the fossils distribution area. The ΔP was more dramatic for ranges that include the area of a wildcard fossil with a distribution area underrepresented among extant taxa. This indicates the importance of including fossils in biogeographic analysis. Exmination of range subdivision at the parental nodes revealed potential range evolution (extinction and dispersal events) along the stems of A. californica and sect. Parryana.

Inferring the biogeographic origins of inter-continental disjunct endemics using a Bayes-DIVA approach

The arcto‐Tertiary relictual flora is comprised of many genera that occur non‐contiguously in the temperate zones of eastern Asia, Europe, eastern North America, and western North America. Within each distributional area, species are typically endemic and may thus be widely separated from closely related species within the other areas. It is widely accepted that this common pattern of distribution resulted from of the fragmentation of a once more‐continuous arcto‐Tertiary forest. The historical biogeographic events leading to the present‐day disjunction have often been investigated using a phylogenetic approach. Limitations to these previous studies have included phylogenetic uncertainty and uncertainty in ancestral range reconstructions. However, the recently described Bayes‐DIVA method handles both types of uncertainty. Thus, we used Bayes‐DIVA analysis to reconstruct the stem lineage distributions for 185 endemic lineages from 23 disjunct genera representing 17 vascular plant families. In particular, we asked whether endemic lineages within each of the four distributional areas more often evolved from (1) widespread ancestors, (2) ancestors dispersed from other areas, or (3) endemic ancestors. We also considered which of these three biogeographic mechanisms may best explain the origins of arcto‐Tertiary disjunct endemics in the neotropics. Our results show that eastern Asian endemics more often evolved from endemic ancestors compared to endemics in Europe and eastern and western North America. Present‐day endemic lineages in the latter areas more often arose from widespread ancestors. Our results also provide anecdotal evidence for the importance of dispersal in the biogeographic origins of arcto‐Tertiary species endemic in the neotropics.

Phylogeny‐based developmental analyses illuminate evolution of inflorescence architectures in dogwoods (Cornus s. l., Cornaceae)

• Inflorescence architecture is important to angiosperm reproduction, but our knowledge of the developmental basis underlying the evolution of inflorescence architectures is limited. Using a phylogeny-based comparative analysis of developmental pathways, we tested the long-standing hypothesis that umbel evolved from elongated inflorescences by suppression of inflorescence branches, while head evolved from umbels by suppression of pedicels. • The developmental pathways of six species of Cornus producing different inflorescence types were characterized by scanning electron microscopy (SEM) and histological analysis. Critical developmental events were traced over the molecular phylogeny to identify evolutionary changes leading to the formation of umbels and heads using methods accounting for evolutionary time and phylogenetic uncertainty. • We defined 24 developmental events describing the developmental progression of the different inflorescence types. The evolutionary transition from paniculate cymes to umbels and heads required alterations of seven developmental events occurring at different evolutionary times. • Our results indicate that heads and umbels evolved independently in Cornus from elongated forms via an umbellate dichasium ancestor and this process involved several independent changes. Our findings shed novel insights into head and umbel evolution concealed by outer morphology. Our work illustrates the importance of combining developmental and phylogenetic data to better define morphological evolutionary processes.

Evolution of bract development and B‐class MADS box gene expression in petaloid bracts of Cornus s. l. (Cornaceae)

Despite increasing interest in the molecular mechanisms of floral diversity, few studies have investigated the developmental and genetic bases of petaloid bracts. This study examined morphological patterns of bract initiation and expression patterns of B-class MADS-box genes in bracts of several Cornus species. We suggest that petaloid bracts in this genus may not share a single evolutionary origin. Developmental pathways of bracts and spatiotemporal expression of B-class genes in bracts and flowers were examined for four closely related dogwood species. Divergent morphological progressions and gene expression patterns were found in the two sister lineages with petaloid bracts, represented by Cornus florida and Cornus canadensis. Phylogeny-based analysis identified developmental and gene expression changes that are correlated with the evolution of petaloid bracts in C. florida and C. canadensis. Our data support the existence of independent evolutionary origins of petaloid bracts in C. canadensis and C. florida. Additionally, we suggest that functional transference within B-class gene families may have contributed to the origin of bract petaloidy in C. florida. However, the underlying mechanisms of petaloid bract development likely differ between C. florida and C. canadensis. In the future this hypothesis can be tested by functional analyses of Cornus B-class genes.

Phylogenomic approaches to deciphering the tree of life

Phylogenomics comprises an interdisciplinary field of comparative biology that uses genomic data to produce phylogenetic relationships among organisms (Philippe et al., 2005; Chan & Ragan, 2013). The term “phylogenomics” was initially applied to studies on gene functions (Eisen, 1998) but subsequently has been widely used to infer the tree of life (Philippe et al., 2004,2005; Pennisi, 2008; Zou et al., 2008; Dos Reis et al., 2012; Liu et al., 2015a, 2015b). With the advent and rapid development of next-generation sequencing (NGS), phylogenomics has gained more popularity in the last few years and is now being employed by many members of the evolutionary and systematics community (Lemmon & Lemmon, 2013; Wen et al., 2013, 2015; Jarvis et al., 2014; Weitemier et al., 2014; Wickett et al., 2014; Zeng et al., 2014).

Recent vicariance and the origin of the rare, edaphically specialized Sandhills lily, Lilium pyrophilum (Liliaceae): evidence from phylogenetic and coalescent analyses

Establishing the phylogenetic and demographic history of rare plants improves our understanding of mechanisms that have led to their origin and can lead to valuable insights that inform conservation decisions. The Atlantic coastal plain of eastern North America harbours many rare and endemic species, yet their evolution is poorly understood. We investigate the rare Sandhills lily (Lilium pyrophilum), which is endemic to seepage slopes in a restricted area of the Atlantic coastal plain of eastern North America. Using phylogenetic evidence from chloroplast, nuclear internal transcribed spacer and two low‐copy nuclear genes, we establish a close relationship between L. pyrophilum and the widespread Turk’s cap lily, L. superbum. Isolation‐with‐migration and coalescent simulation analyses suggest that (i) the divergence between these two species falls in the late Pleistocene or Holocene and almost certainly post‐dates the establishment of the edaphic conditions to which L. pyrophilum is presently restricted, (ii) vicariance is responsible for the present range disjunction between the two species, and that subsequent gene flow has been asymmetrical and (iii) L. pyrophilum harbours substantial genetic diversity in spite of its present rarity. This system provides an example of the role of edaphic specialization and climate change in promoting diversification in the Atlantic coastal plain.

Phylogenomics of polyploid Fothergilla (Hamamelidaceae) by RAD‐tag based GBS—insights into species origin and effects of software pipelines

Fothergilla (Hamamelidaceae) consists of Fothergilla gardenii (4x) from the coastal plains of the southeastern USA, F. major (6x) from the piedmont and mountains of the same region, and a few allopatric diploid populations of unknown taxonomic status. The objective of this study was to explore the relationships of the polyploid species with the diploid plants. Genotyping by sequencing (GBS) was applied to generate genome‐wide molecular markers for phylogenetic and genetic structure analyses of 36 accessions of Fothergilla. Sanger sequencing of three plastid and one nuclear regions provided data for comparison with GBS‐based results. Phylogenetic outcomes were compared using data from different sequencing runs and different software workflows. The different data sets showed substantial differences in inferred phylogenies, but all supported a genetically distinct 6x F. major and two lineages of the diploid populations closely associated with the 4x F. gardenii. We hypothesize that the 4x F. gardenii originated through hybridization between the Gulf coastal 2x and an extinct (or undiscovered) 2x lineage, followed by backcrosses to the Atlantic coastal 2x before chromosome doubling, and the 6x F. major also originated from the “extinct” 2x lineage. Alternative scenarios are possible but are not as well supported. The origins and divergence of the polyploid species likely occurred during the Pleistocene cycles of glaciation, although fossil evidence indicates the genus might have existed for a much longer time with a wider past distribution. Our study demonstrates the power of combining GBS data with Sanger sequencing in reconstructing the evolutionary network of polyploid lineages.

Evidence for range stasis during the latter Pleistocene for the Atlantic Coastal Plain endemic genus, Pyxidanthera Michaux

The general phylogeographical paradigm for eastern North America (ENA) is that many plant and animal species retreated into southern refugia during the last glacial period, then expanded northward after the last glacial maximum (LGM). However, some taxa of the Gulf and Atlantic Coastal Plain (GACP) demonstrate complex yet recurrent distributional patterns that cannot be explained by this model. For example, eight co‐occurring endemic plant taxa with ranges from New York to South Carolina exhibit a large disjunction separating northern and southern populations by >300 km. Pyxidanthera (Diapensiaceae), a plant genus that exhibits this pattern, consists of two taxa recognized as either species or varieties. We investigated the taxonomy and phylogeography of Pyxidanthera using morphological data, cpDNA sequences, and amplified fragment length polymorphism markers. Morphological characters thought to be important in distinguishing Pyxidanthera barbulata and P. brevifolia demonstrate substantial overlap with no clear discontinuities. Genetic differentiation is minimal and diversity estimates for northern and southern populations of Pxyidanthera are similar, with no decrease in rare alleles in northern populations. In addition, the northern populations harbour several unique cpDNA haplotypes. Pyxidanthera appears to consist of one morphologically variable species that persisted in or near its present range at least through the latter Pleistocene, while the vicariance of the northern and southern populations may be comparatively recent. This work demonstrates that the refugial paradigm is not always appropriate and GACP endemic plants, in particular, may exhibit phylogeographical patterns qualitatively different from those of other ENA plant species.

Intercontinental and intracontinental biogeography—patterns and methods

Intercontinental and intracontinental biogeography— patterns and methods 1Jun WEN∗ 2Qiu-Yun (Jenny) XIANG 3Hong QIAN 4Jianhua LI 5Xiao-Quan WANG 6Stefanie M. ICKERT-BOND 1(Department of Botany, MRC-166, Smithsonian Institution, PO Box 37012, Washington DC 20013-7012, USA) 2(Department of Plant Biology, North Carolina State University, Raleigh, NC 27695-7612, USA) 3(Research and Collections Center, Illinois State Museum, Springfield, IL 62703, USA) 4(Biology Department, Hope College, Holland, MI 49423, USA) 5(State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China) 6(UA Museum of the North Herbarium and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, AK 99775-6960, USA)

Ecological genomics of local adaptation in Cornus florida L. by genotyping by sequencing

Abstract Discovering local adaptation, its genetic underpinnings, and environmental drivers is important for conserving forest species. Ecological genomic approaches coupled with next‐generation sequencing are useful means to detect local adaptation and uncover its underlying genetic basis in nonmodel species. We report results from a study on flowering dogwood trees (Cornus florida L.) using genotyping by sequencing (GBS). This species is ecologically important to eastern US forests but is severely threatened by fungal diseases. We analyzed subpopulations in divergent ecological habitats within North Carolina to uncover loci under local selection and associated with environmental–functional traits or disease infection. At this scale, we tested the effect of incorporating additional sequencing before scaling for a broader examination of the entire range. To test for biases of GBS, we sequenced two similarly sampled libraries independently from six populations of three ecological habitats. We obtained environmental–functional traits for each subpopulation to identify associations with genotypes via latent factor mixed modeling (LFMM) and gradient forests analysis. To test whether heterogeneity of abiotic pressures resulted in genetic differentiation indicative of local adaptation, we evaluated F st per locus while accounting for genetic differentiation between coastal subpopulations and Piedmont‐Mountain subpopulations. Of the 54 candidate loci with sufficient evidence of being under selection among both libraries, 28–39 were Arlequin–BayeScan F st outliers. For LFMM, 45 candidates were associated with climate (of 54), 30 were associated with soil properties, and four were associated with plant health. Reanalysis of combined libraries showed that 42 candidate loci still showed evidence of being under selection. We conclude environment‐driven selection on specific loci has resulted in local adaptation in response to potassium deficiencies, temperature, precipitation, and (to a marginal extent) disease. High allele turnover along ecological gradients further supports the adaptive significance of loci speculated to be under selection.