Campanula in Western North America Eric G
Total Page：16
File Type：pdf, Size：1020Kb
Integrating environmental, molecular, and morphological data to unravel an ice-age radiation of arctic-alpine Campanula in western North America Eric G. DeChaine1, Barry M. Wendling1 & Brenna R. Forester2 1Department of Biology, Western Washington University, 516 High St., Bellingham, Washington 98225 2University Program in Ecology, Nicholas School of the Environment, Duke University, Box 90328, Durham, North Carolina 27708 Keywords Abstract Arctic-alpine plants, ecological niche modeling, morphology, Pacific Northwest, Many arctic-alpine plant genera have undergone speciation during the Quater- Quaternary, statistical phylogeography. nary. The bases for these radiations have been ascribed to geographic isolation, abiotic and biotic differences between populations, and/or hybridization and Correspondence polyploidization. The Cordilleran Campanula L. (Campanulaceae Juss.), a Eric G. DeChaine monophyletic clade of mostly endemic arctic-alpine taxa from western North Department of Biology, Western Washington America, experienced a recent and rapid radiation. We set out to unravel the University, 516 High St., Bellingham, WA factors that likely influenced speciation in this group. To do so, we integrated 98225. Tel: 360-650-6575; Fax: 360-650-3148; environmental, genetic, and morphological datasets, tested biogeographic E-mail: [email protected] hypotheses, and analyzed the potential consequences of the various factors on the evolutionary history of the clade. We created paleodistribution models to Funding Information identify potential Pleistocene refugia for the clade and estimated niche space for Funding was provided by the National individual taxa using geographic and climatic data. Using 11 nuclear loci, we Science Foundation (ARC-0714232 and DEB- reconstructed a species tree and tested biogeographic hypotheses derived from 1256832). the paleodistribution models. Finally, we tested 28 morphological characters, Received: 19 May 2014; Revised: 18 June including floral, vegetative, and seed characteristics, for their capacity to differ- 2014; Accepted: 19 June 2014 entiate taxa. Our results show that the combined effect of Quaternary climatic variation, isolation among differing environments in the mountains in western North America, and biotic factors influencing floral morphology contributed to speciation in this group during the mid-Pleistocene. Furthermore, our biogeo- doi: 10.1002/ece3.1168 graphic analyses uncovered asynchronous consequences of interglacial and glacial periods for the timing of refugial isolation within the southern and northwestern mountains, respectively. These findings have broad implications for understanding the processes promoting speciation in arctic-alpine plants and the rise of numerous endemic taxa across the region. Introduction known for a relatively high number of Pleistocene specia- tion events (reviewed in Brochmann and Brysting 2008). The dynamic interplay between the climatic variability of The main modes of genetic divergence and speciation the glacial cycles and the rugged topography of mountain in plants were heightened for the arctic-alpine flora dur- landscapes provided many opportunities for the diversifi- ing the Quaternary. First, isolation over many genera- cation and speciation of arctic-alpine plants during the tions, whether between glacial refugia or interglacial sky Quaternary (Abbott et al. 2000). Whether or not the islands, promoted genetic differentiation through genetic Pleistocene promoted speciation is under debate (Haffer drift. For some taxa, new species arose simply through 1969; Avise et al. 1998; Schoville et al. 2012). In the case isolation in the absence of ecological differentiation of arctic-alpine plants, it is clear that speciation did occur (Kadereit et al. 2004; Valente et al. 2010). That said the and is ongoing today. Indeed, the Arctic is no longer vast majority of studies to date have highlighted the thought of as an evolutionary “freezer” as posited by importance of remixing, hybridization, and polyploidiza- some (e.g., Allen et al. 2006), but rather the flora is tion following isolation in the process of recent ª 2014 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 1 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Rapid Radiation of Cordilleran Campanula E. G. DeChaine et al. arctic-alpine plant speciation (Brochmann et al. 2004). Cordilleran Campanula, comprised of approximately Finally, environmental conditions and biotic communities seven mostly endemic species, experienced a rapid radia- likely varied among refugia, and the different selective tion after colonization of North America in the Pleisto- pressures imposed by those environments provided the cene (Wendling et al. 2011). Members of this clade are opportunity for ecological speciation (reviewed in Givnish patchily distributed along the fragmented mountain land- 2010). This includes not only abiotic, but also biotic factors scape of the west, ranging from the Brooks Range of – variation among the available pollinators would have been Alaska (and eastern Siberia) southwards along the Coast, of particular importance to plant reproduction, divergence, Cascade, Olympic, and Rocky Mountain ranges to north- and floral evolution (Grant 1949; Nakazato et al. 2013). The ern California and southern Colorado. In addition, several aforementioned factors could have acted independently or other genera within the Campanulaceae, including in concert to promote genetic divergence. Triodanis Raf. ex Greene and the Campanula-Githopsis The western region of North America is geographically Nutt.-Heterocodon Nutt. clade, have diversified in North complex with a high degree of environmental heterogene- America (Morin 1983). The reoccurring theme of coloni- ity, affording plants a number of unique habitat types zation, diversification, and endemism begs the question as and biotic interactions. Accordingly, 60% of the vascular to what ecological and evolutionary forces have brought plant genera endemic to North America are limited to the about this pattern. Geographic isolation has been cited as western portion of the continent (Qian et al. 2007). Dur- the basis for genetic divergence and endemism in some ing glacial episodes, massive sheets of ice grew over much Campanula clades (Cellinese et al. 2009; Haberle et al. of the continent, and in conjunction with the expansion 2009). Exposure to different environmental conditions of mountain glaciers, isolated regions and their inhabit- has also likely played a role in speciation within the fam- ants. Several potential glacial refugia have been identified ily. In addition to abiotic factors, floral morphological in the west, including Beringia, Haida Gwaii, Vancouver diversity in Campanula has been driven in large part by Island, the Olympic Peninsula, the Southern Cascades pollinator-mediated selection on floral traits (Roquet (including the Columbia Gorge and the Klamath region), et al. 2008; Scheepens et al. 2011), and this could be a and the Northern and Southern Rocky Mountains factor in the diversification within the Cordilleran Cam- (Hulten 1937; Soltis et al. 1997; Swenson and Howard panula as well. It is important to note that the various 2005; Shafer et al. 2010). Furthermore, the north–south factors promoting genetic divergence and speciation are running cordillera provided opportunities for the persis- not mutually exclusive, but are potentially all pieces of tence of arctic-alpine plants during cold and warm cli- the evolutionary puzzle for the radiation of some arctic- matic periods (Allen et al. 2012; DeChaine et al. 2013a,b; alpine Campanula clades during the Quaternary. Marr et al. 2013). In general, during interglacials, popula- The objective of our study was to investigate the factors tions expanded from refugia, but along a chain of sky that promoted the recent and rapid radiation of the Cor- islands that reduced the connectedness among alpine dilleran Campanula (see Fig. 1 for an image of C. lasio- populations and potentially led to local extinction carpa Cham., a member of this clade). Specifically, we through habitat reduction. Thus, isolation among popula- asked what stimulated speciation in this clade. As such, tions likely impacted the evolution and diversification of our study was focused at the species level, and we did not arctic-alpine taxa during both glacial and interglacial investigate the infraspecific (e.g., population genetic) stages. Additionally, environmental conditions, resources, diversity within each taxon. To accomplish this goal, we communities, and biotic interactions have varied along took an integrated approach to examining the speciational the length of the cordillera. The high proportion of geo- history of this group. First, we created paleodistribution graphically limited species of mountain plants in western ecological niche models (ENMs) and identified potential North America is likely a product of the interplay Pleistocene refugia (regions that likely harbored suitable between climate and topography and the associated cycles habitat throughout the Pleistocene) for the clade, which of isolation and admixture among neighboring popula- were then used to generate biogeographic hypotheses [(1) tions (DeChaine et al. 2013a,b). multiple refugia, (2) northward expansion from a south- The arctic-alpine Campanula L. (Campanulaceae Juss.) ern refugium, and (3)