Diploid Hybrid Origin of Ostryopsis Intermedia (Betulaceae) in the Qinghai-Tibet Plateau Triggered by Quaternary Climate Change
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Molecular Ecology (2014) 23, 3013–3027 doi: 10.1111/mec.12783 Diploid hybrid origin of Ostryopsis intermedia (Betulaceae) in the Qinghai-Tibet Plateau triggered by Quaternary climate change BINGBING LIU,*† RICHARD J. ABBOTT,‡ ZHIQIANG LU,† BIN TIAN† and JIANQUAN LIU* *MOE Key Laboratory of Bio-Resources and Eco-Environment, College of Life Science, Sichuan University, Chengdu 610065, China, †State Key Laboratory of Grassland Agro-Ecosystem, College of Life Science, Lanzhou University, Lanzhou 730000, China, ‡School of Biology, University of St Andrews, Mitchell Building, St Andrews, Fife, KY16 9TH, UK Abstract Despite the well-known effects that Quaternary climate oscillations had on shaping intraspecific diversity, their role in driving homoploid hybrid speciation is less clear. Here, we examine their importance in the putative homoploid hybrid origin and evolu- tion of Ostryopsis intermedia, a diploid species occurring in the Qinghai-Tibet Plateau (QTP), a biodiversity hotspot. We investigated interspecific relationships between this species and its only other congeners, O. davidiana and O. nobilis, based on four sets of nuclear and chloroplast population genetic data and tested alternative speciation hypotheses. All nuclear data distinguished the three species clearly and supported a close relationship between O. intermedia and the disjunctly distributed O. davidiana. Chloroplast DNA sequence variation identified two tentative lineages, which distin- guished O. intermedia from O. davidiana; however, both were present in O. nobilis. Admixture analyses of genetic polymorphisms at 20 SSR loci and sequence variation at 11 nuclear loci and approximate Bayesian computation (ABC) tests supported the hypothesis that O. intermedia originated by homoploid hybrid speciation from O. davidiana and O. nobilis. We further estimated that O. davidiana and O. nobilis diverged 6–11 Ma, while O. intermedia originated 0.5–1.2 Ma when O. davidiana is believed to have migrated southward, contacted and hybridized with O. nobilis possi- bly during the largest Quaternary glaciation that occurred in this region. Our findings highlight the importance of Quaternary climate change in the QTP in causing hybrid speciation in this important biodiversity hotspot. Keywords: climate change, homoploid hybrid speciation, Ostryopsis, Qinghai-Tibet Plateau Received 14 February 2014; revision received 18 April 2014; accepted 25 April 2014 hybridization and introgression (Comes & Kadereit Introduction 1998; Avise 2000; Bennett 2004; Mallet 2008; Wang et al. It is well known that Quaternary climate oscillations 2009). In some instances, this will have triggered the played an important role in altering patterns of biodi- origin of new hybrid species through either homoploid versity in many parts of the world by causing changes hybrid speciation or allopolyploidy (Comes & Kadereit in species abundance and distribution (Hewitt 1999; 1998; Abbott & Brochmann 2003; Anton et al. 2013; Sun Provan & Bennett 2008). Shifts in species distributions et al. 2014). Although numerous plant species are will have led, on occasion, to secondary contact thought to have originated by allopolyploidy, there are between closely related species that were previously currently very few known cases of homoploid hybrid distributed allopatrically leading to interspecific speciation having occurred during the Quaternary (Sol- tis & Soltis 2009; Nolte & Tautz 2010; Abbott & Riese- Correspondence: Jianquan Liu, Fax: +86 028-85412571; berg 2012). This might be partly because homoploid E-mail: [email protected] or [email protected] hybrid speciation is more difficult to detect than © 2014 John Wiley & Sons Ltd 3014 B. LIU ET AL. allopolyploid speciation, due to the absence of easily 2010). In addition, new niches created by QTP uplifts, observed changes in chromosome number (Rieseberg and Quaternary climatic oscillations in this climate-sen- et al. 2003; James & Abbott 2005). However, with the sitive region may have also favoured homoploid hybrid increased availability of DNA sequencing and recently speciation, although only two diploid hybrid species developed analytical procedures, it is becoming easier (both conifers) have been reported so far from the QTP to detect homoploid hybrid species, their dates of origin (Ma et al. 2006; Sun et al. 2014). Clearly, more studies and subsequent demographic changes (Gross & Riese- (especially on angiosperms) need to be conducted on berg 2005; Howarth & Baum 2005; Abbott et al. 2010; candidate homoploid hybrid species in this region Salazar et al. 2010; Wang et al. 2011; Clay et al. 2012; before conclusions are reached on whether or not ho- Gao et al. 2012) although alternative hypotheses of moploid hybrid speciation was an important mecha- hybrid speciation vs. other patterns are rarely tested nism of speciation in the QTP during the Quaternary. (but see Sun et al. 2014). Here, we focus on the species, Ostryopsis intermedia,a Here, we use nuclear and chloroplast DNA sequence shrub that is considered to be possibly a homoploid variation together with approximate Bayesian computa- hybrid species derived from O. nobilis, which is distrib- tion (ABC) and niche modelling to examine the possible uted in the southeast (SE) part of the QTP, and O. davi- homoploid hybrid origin of Ostryopsis intermedia (Betul- diana, which is currently disjunctly distributed in aceae), which is endemic to the Qinghai-Tibet Plateau northern China (Fig. 1a; Tian et al. 2010). These three (QTP), China (Fig. 1a). The QTP and adjacent regions species are diploid (2n = 16) and show strong clonal comprise one of the world’s biodiversity hotspots for propagation through the production of underground conservation priorities (Myers et al. 2000). More than rhizomes (Li & Skvortsov 1999; Tian et al. 2009). They 9000 vascular plant species occur in this region, and are the only representatives of the genus Ostryopsis. approximately 18% are endemic (Wu 2008). The genera- Our test of the homoploid hybrid origin hypothesis tion of these endemics may have been largely driven by of O. intermedia involved a combination of several rapid and continuous uplifts of the QTP since the Mio- approaches. Initially, we surveyed the nuclear ribo- cene (Harrison et al. 1992; Li et al. 1995; Shi et al. 1998; somal internal transcribed spacer (ITS) and cpDNA An et al. 2001), which are likely to have accelerated allo- sequence variation among individuals of each species to patric speciation in the region (Liu et al. 2006; Xu et al. examine interspecific relationships and to estimate (a) (b) (d) 58 72 82 108 170 171 172 225 395 484 565 582 586 C4 G C A C G T - C C G C A C C3 - T A C G T - T C G C A T C6 C1 C7 - - G T A C A C T C T G T C2 C5 (c) (e) 60 40 20 0 (MA) (MA)0 20 40 60 O. davidiana Qinghai-Tibet Plateau O. intermedia O. nobilis Ostrya Ostrya Carpinus Carpinus Corylus Corylus Betula Betula Alnus Alnus Fig. 1 Current geographical distributions of Ostryopsis davidiana (north), O. intermedia (southwest) and O. nobilis (southeast), plus phylogenetic relationships among their chloroplast haplotypes (chlorotypes) and nuclear internal transcribed spacer (ITS) genotypes. (a) Species geographical ranges; (b) ITS sequence variation between three species; (d) median-joining network of chlorotypes recov- ered from the three species; (c) phylogenetic relationship among the three species based on ITS genotypes; and (e) cpDNA chloro- types. Bayesian estimates of dates of divergence are indicated for key nodes of phylogenies. Colours indicate species as for distributions. Relative sizes of circles for chlorotypes in (d) are proportional to chlorotype frequencies, while solid dots indicate miss- ing chlorotypes. In the phylogenies (c) and (e), solid branches indicate Bayesian posterior probabilities >0.95. © 2014 John Wiley & Sons Ltd DIPLOID HYBRID SPECIATION OF OSTRYOPSIS 3015 divergence times of the different lineages detected. We Finally, we used 20 pairs of nuclear simple sequence next examined sequence variation of 11 nuclear loci, repeat (SSR) markers (five from Ma et al. 2013a and 15 and genetic polymorphisms generated by 20 nuclear from Liu et al. 2014) to examine interspecific differentia- simple sequence repeat (SSR) markers to confirm inter- tion and relationships further. specific relationships. We then tested the mode of origin of O. intermedia utilizing an ABC approach conducted Phylogenetic analyses and divergence estimation on the population genetic data obtained from the 11 nuclear loci sequences and 20 SSRs. Finally, we used Phylogenetic relationships and divergence times Bayesian inference methods and species distribution between lineages based on ITS and cpDNA sequence models (SDMs) to model demographic shifts of the variation were estimated using Bayesian inference three species in response to Quaternary climate change methods implemented in BEAST version 1.8.0 (Drum- to determine whether the distributions of the two puta- mond et al. 2012). One genus closely related to Betula- tive parental species could have overlapped in the past, ceae, Ticodendron, was selected as outgroup. The best-fit allowing interspecific hybridization and hybrid specia- model of nucleotide substitution for each locus was esti- tion to have occurred. Thus, our research aimed to mated using the Akaike information criterion (AIC) in address the following questions: (i) Does O. intermedia the program JMODELTEST version 2.1.4 (Darriba et al. represent a genetically independent and ecologically 2012). All indels were treated as missing in