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Spreading Winge and flying high: The evolutionary importance of polyploidy after a century of study
Since the discovery of polyploidy in plants just more than a century ago, research on polyploidy is as vigorous as ever. At the Botany 2015 meeting in Edmonton, Alberta, six researchers participated in the symposium “The Evolutionary Importance of Polyploidy” to address recent debates on polyploid speciation. These authors are joined by others in this special issue of the American Journal of Botany to highlight recent advances in polyploid research. The 19 articles collected here represent a diverse range of research from established and nascent scientists. Here we provide a guide to the articles in this issue and highlight their major results.
Perhaps no topic of study has received a greater boost from the genomics era than polyploidy. Speciation by genome duplication was recognized early in the study of evolutionary genetics and “represented the first major triumph in the genetics of speciation” (Coyne and Orr, 2004, p. 322). Plants with sets of doubled chromosomes were encountered in early cytological studies (Lutz, 1907), and Winge (1917) provided one of the most influential hypotheses for the origins of these numbers. He proposed the now familiar concept that these polyploid plants were fertile because genome doubling restored chromosome pairing in otherwise sterile hybrids. The restoration of fertility to sterile hybrids by doubling their genomes was a potent and elegant demonstration of how postzygotic reproductive isolation could be solved (Clausen and Goodspeed, 1925). Further support for Winge’s hypothesis came from Müntzing (1930) who recreated a naturally occurring polyploid species. These studies demonstrated one of the first mechanisms of how new species may arise from genomic changes of existing species. The pioneering polyploidy research of these botanists played a leading role in shaping research on speciation genetics. Their experiments even inspired a young Dobzhansky (1933) to test whether polyploidy restored fertility to sterile fruit flies (it did not). By the time of the modern synthesis, polyploidy was already a relatively well-studied topic and recognized as the biggest difference between plant and animal speciation (Dobzhansky, 1937)—and was the most shocking and important correction to Darwin’s theory of the origin of species (Haldane, 1959).
By the latter half of the 20th century, however, polyploidy had been relegated as largely unimportant by many researchers. Many plant species were certainly recognized to have polyploid origins (Stebbins, 1950; Grant, 1981), but the prevalence and persistence of diploids raised questions about the evolutionary contribution of polyploidy (Stebbins, 1971). Although ancient polyploidy was hypothesized and implicitly recognized in many “basic” chromosome number estimates (Stebbins, 1950, 1971; Klekowski and Baker, 1966; Ohno, 1970; Grant, 1981), many biologists came to regard polyploidy as “evolutionary noise” (Wagner, 1970). During his talk at the Botany 2015 symposium on polyploidy, Doug Soltis recounted that as a young researcher he was told to avoid polyploidy because it was a black hole of research! Today such advice would probably not be given. Research beginning with the molecular era revealed that even plants with high chromosome numbers have diploid patterns of gene expression (Gastony and Gottlieb, 1982; Gastony and Darrow, 1983; Barker and Wolf, 2010; Haufler, 2014). One hypothesis proposed to explain these patterns of chromosome number and gene expression was diploidization following ancient polyploidy (Stebbins, 1985; Haufler and Soltis, 1986; Haufler, 1987; Gastony, 1991). Analyses of numerous plant (Vision et al., 2000; Bowers et al., 2003; Blanc and Wolfe, 2004; Cui et al., 2006; Jaillon et al., 2007; Barker et al., 2008, 2009, 2012, 2016b; Rensing et al., 2008; Soltis et al., 2009; Schmutz et al., 2010; Shi et al., 2010; Tang et al., 2010; Velasco et al., 2010; Wang et al., 2011; Rodgers-Melnick et al., 2012; Tomato Genome Consortium, 2012; Amborella Genome Project, 2013; Barker, 2013; Chalhoub et al., 2014; Kagale et al., 2014; Liu et al., 2014; Vanneste et al., 2014; Edger et al., 2015; Marques et al., 2016), animal (Gregory and Mable, 2005; Santini et al., 2009; Hallinan and Lindberg, 2011; Cañestro et al., 2013; Berthelot et al., 2014; McLysaght et al., 2014; Nossa et al., 2014; Clarke et al., 2015; Pasquier et al., 2016), and other eukaryotic genomes (Aury et al., 2006; Scannell et al., 2006; Fares et al., 2013; Conant, 2014; McGrath et al., 2014; Scienski et al., 2015) revealed that many eukaryotes do indeed have a polyploid ancestry. Although there have been recent debates on the average fate of polyploid species (Mayrose et al., 2011, 2015; Soltis et al., 2014a), there is consensus that polyploidy has contributed to the evolution of nearly all lineages of vascular plants (Jiao et al., 2011; Arrigo and Barker, 2012; Soltis et al., 2014b; Li et al., 2015; Wendel, 2015) and that polyploids comprise a large fraction of contemporary plant diversity (Wood et al., 2009; Soltis et al., 2010; Mayrose et al., 2011; Scarpino et al., 2014; Barker et al., 2016a).
The resurgence of interest in polyploidy over the past 15 yr has been dramatic. Although polyploidy has long been a favored topic of many botanists, the Botany 2000 meeting of the Botanical Society of America in Portland, Oregon, featured only six abstracts, or 1% of the total, with “polyploidy” as a key word (Fig. 1). At Botany 2015, 36 talks and posters listed “polyploidy” as a key word, for 3% of the total. Although 3% may seem like a relatively small fraction of the submissions, polyploidy was the third-ranked key word at Botany 2015. Only submissions on “phylogeny” with 59 and “fungi” with 37 ranked higher than those on “polyploidy”. Polyploidy will likely remain an important topic in the near future as botanists continue to explore the consequences of polyploidy at multiple scales of ecology and time.
Nearly a century after Winge’s (1917) landmark publication, research on polyploidy remains vibrant and diverse. Although frequently discussed as a topic of genome research, polyploidy impacts the biology of plants in many dimensions. Many of these different avenues of polyploid research are featured in this special issue of the American Journal of Botany. The 19 papers published in this special issue provide a snapshot of the breadth of research on polyploidy in plants. We have organized the manuscripts into three thematic areas to aid navigation of the research discussed in this special issue. These include papers on the evolutionary consequences of polyploidy, the origins of polyploid species, and the impacts of polyploidy on plant ecology. Next, we highlight the major findings of these papers and place them in context.