The impact of floral morphology on genetic differentiation in two closely related biennial plant species

AoB PLANTS, Sep 2018

The genetic diversity and structure of plant populations are determined by the interaction of three distinct processes: gene flow, genetic drift and natural selection. These processes are to some extent dependent on the mating system of plants, which in turn is largely determined by floral morphology and the level of herkogamy in particular. In this study, we used molecular markers to investigate the impact of floral morphology on genetic differentiation and structure in two closely related Centaurium species that display large variation in floral morphology across two distinct geographic regions in Europe (mainland Europe and the UK). Our results showed that genetic differences between regions and populations within regions were similar for both species, but that patterns of genetic structure largely depended on the observed variation in floral morphology. Populations of Centaurium erythraea showed higher genetic differentiation and clear isolation by distance (IBD) in mainland Europe, but limited IBD in the UK. Opposite patterns were found in Centaurium littorale, with higher genetic differentiation and significant IBD in populations sampled in the UK and lower genetic differentiation in Continental populations with no pattern of IBD. Overall, these results indicate that variation in floral morphology has a profound impact on structuring of genetic diversity, with populations displaying low levels of herkogamy showing the strongest patterns of genetic structuring and the reverse pattern in populations showing high levels of herkogamy.

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The impact of floral morphology on genetic differentiation in two closely related biennial plant species

Abstract The genetic diversity and structure of plant populations are determined by the interaction of three distinct processes: gene flow, genetic drift and natural selection. These processes are to some extent dependent on the mating system of plants, which in turn is largely determined by floral morphology and the level of herkogamy in particular. In this study, we used molecular markers to investigate the impact of floral morphology on genetic differentiation and structure in two closely related Centaurium species that display large variation in floral morphology across two distinct geographic regions in Europe (mainland Europe and the UK). Our results showed that genetic differences between regions and populations within regions were similar for both species, but that patterns of genetic structure largely depended on the observed variation in floral morphology. Populations of Centaurium erythraea showed higher genetic differentiation and clear isolation by distance (IBD) in mainland Europe, but limited IBD in the UK. Opposite patterns were found in Centaurium littorale, with higher genetic differentiation and significant IBD in populations sampled in the UK and lower genetic differentiation in Continental populations with no pattern of IBD. Overall, these results indicate that variation in floral morphology has a profound impact on structuring of genetic diversity, with populations displaying low levels of herkogamy showing the strongest patterns of genetic structuring and the reverse pattern in populations showing high levels of herkogamy. AFLP, Centaurium erythraea, Centaurium littorale, floral morphology, geographic variation, herkogamy, isolation by distance, population structure Introduction The genetic diversity and structure of plant populations are determined by the interaction of gene flow, genetic drift and natural selection, processes that are influenced by the geographic distribution of plant populations and population demography (Eckert et al. 2008). Historical events such as glaciation or orogeny determine to a large extent the geographic ranges of plant and animal species, which in turn are determined by geographic barriers that limit or prevent further dispersal (e.g. mountains, oceans, or more recently also fragmentation caused by human activities) (Slatkin 1987; Eckert et al. 2008; Zhang et al. 2014). Furthermore, environmental conditions often change gradually over a geographic gradient, not only determining the species that can live at a certain location, but also potentially leading to within-species variation by selecting for individuals that are genetically more adapted to specific conditions (Harrison 2006; Eckert et al. 2008). For example, temperature and humidity are strongly related to altitude or latitude and are both correlated with variation in plant functional traits, such as plant size (Li et al. 1998), leaf morphology (Meinzer et al. 1985; Byars et al. 2007) and flower morphology (Olsson and Ågren 2002; Levin 2010; 2012) within one species. Differences in environmental pressures have been shown to influence plant mating systems, a major determinant of population genetic structure (Hamrick and Godt 1996; Arnaud-Haond et al. 2006; Honnay and Jacquemyn 2007; Aguilar et al. 2008; Soengas et al. 2013; Pettengill et al. 2016). Mating systems can show strong variation, even within a single species, ranging from fully outcrossing to entirely selfing (Schemske and Lande 1985; Barrett 2002; Goodwillie et al. 2005; Wright et al. 2013). Due to the effects of genetic drift, selfing populations are expected to be more homozygous and to be genetically less diverse than populations of outcrossing species (Schoen and brown 1991; Charlesworth and Charlesworth 1995; Williams 2001). Outcrossing populations, on the other hand, are expected to show reduced population structure due to higher gene flow via pollen (Stebbins 1957; Wright et al. 2013; Pettengill et al. 2016). As a result, outcrossing populations are more likely to show patterns of isolation by distance (IBD), with less gene flow between more distant populations. In contrast, a flat relationship with high variance between genetic and geographic distance can be expected when comparing selfing populations due to limited gene flow and the stochastic effects of genetic drift, even when populations are adjacent (Hutchison and Templeton 1999; Pettengill et al. 2016). Selfing rates are strongly determined by flower characteristics such as flowering time and floral morphology (Wyatt 1982; Murawski and Hamrick 1992; Harder and Barrett 1996). One of the floral characteristics that has been demonstrated to have a major influence on selfing rates in self-compatible plants and to be under strong selection is herkogamy, i.e. the spatial separation of anthers and stigmas within a flower (Jacquemyn et al. 2012; Cheptou et al. 2017; Opedal et al. 2017; Toräng et al. 2017). Decreasing levels of stigma–anther segregation generally lead t (...truncated)


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Mertens, Arne, Brys, Rein, Schouppe, Dorien, Jacquemyn, Hans. The impact of floral morphology on genetic differentiation in two closely related biennial plant species, AoB PLANTS, 2018, Volume 10, Issue 5, DOI: 10.1093/aobpla/ply051