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The Evolutionary History of Antirrhinum Suggests That Ancestral Phenotype Combinations Survived Repeated Hybridizations

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The Evolutionary History of Antirrhinum Suggests That Ancestral Phenotype Combinations Survived Repeated Hybridizations The Plant Journal (2011) 66, 1032–1043 doi: 10.1111/j.1365-313X.2011.04563.x The evolutionary history of Antirrhinum suggests that ancestral phenotype combinations survived repeated hybridizations Yvette Wilson and Andrew Hudson*,† Institute of Molecular Plant Sciences, University of Edinburgh, King’s Buildings, Mayfield Road, Edinburgh EH9 3JH, UK Received 29 November 2010; revised 25 February 2011; accepted 1 March 2011; published online 6 April 2011. *For correspondence (fax +44 131 650 5392; e-mail [email protected]). †Present address: Division of Plant Science, University of Dundee at SCRI, Invergowrie, Dundee, DD2 5DA, UK. SUMMARY The model species Antirrhinum majus (the garden snapdragon) has over 20 close wild relatives that are morphologically diverse and adapted to different Mediterranean environments. Hybrids between Antirrhinum species have been used successfully to identify genes underlying their phenotypic differences, and to infer how selection acts on them. To better understand the genetic basis for this diversity, we have examined the evolutionary relationships between Antirrhinum species and how these relate to geography and patterns of phenotypic variation in the genus as a whole. Large population samples and both plastid and multilocus nuclear genotypes resolved the relationships between many species and provided some support for the traditional taxonomic division of the genus into morphological subsections. Morphometric analysis of plants grown in controlled conditions supported the phenotypic distinction of the two largest subsections, and the involvement of multiple underlying genes. Incongruence between nuclear and plastid genotypes further suggested that several species have arisen after hybridization between subsections, and that some species continue to hybridize. However, all potential hybrids appear to have retained a phenotype similar to one of their ancestors, suggesting that ancestral combinations of characters are maintained by selection at many different loci. Keywords: Antirrhinum, snapdragon, phylogeny, morphological evolution. INTRODUCTION Much of our understanding of the genes involved in mor- genus Antirrhinum – in which between 17 and 27 distinct phological evolution and speciation has come from taxa that species and subspecies have been recognized in different are sufficiently different to be regarded as separate species, taxonomic accounts (Rothmaler, 1956; Webb, 1971; Sutton, but that retain the ability to form fertile hybrids. Both natural 1988). Although morphologically diverse and adapted to and artificial hybrids have been used to detect loci underly- different, often extreme, environments, all Antirrhinum ing differences between the parental species. In some cases, species can form fertile hybrids with each other and with the genes and mutations have themselves been identified. A. majus when artificially cross-pollinated. Such hybrids This has been particularly successful when the research have identified genes underlying differences in morphology infrastructure developed in a closely related model species and flower colour between their parents (Hackbarth et al., is available, for example in Drosophila (McGregor et al., 1942; Langlade et al., 2005; Schwinn et al., 2006; Feng et al., 2007; Jeong et al., 2008). 2009). Natural Antirrhinum hybrids have also identified The garden snapdragon, Antirrhinum majus (Plantagina- genes involved in flower colour variation, and have sug- ceae) has been used as a model to study inheritance, and the gested how selection acts on them (Whibley et al., 2006). genetic control of development and flower colour (Schwarz- The genus Antirrhinum can therefore provide a model for Sommer et al., 2003). Its close relatives are native to the understanding the genetic basis for patterns of phenotypic western Mediterranean region, mostly the Iberian peninsu- diversity and adaptation around the species level, which lar, and comprise a monophyletic group – the traditional may be typical of many recently evolved Mediterranean 1032 ª 2011 The Authors The Plant Journal ª 2011 Blackwell Publishing Ltd Constrained evolution in the genus Antirrhinum 1033 taxa (Thompson, 2005). However, it has been difficult to relate the genetic differences between pairs of parental species to variation in the genus as a whole because the relationships between Antirrhinum species have not been resolved. For instance, it is currently not possible to infer the ancestral state of a character and whether similar pheno- types might have evolved multiple times within the genus. One obstacle to resolving evolutionary relationships within Antirrhinum is reflected in the unclear taxonomy of its species, many of which have not been reported to have a unique, fixed character (a synapomorphy; Webb, 1971). Therefore, species might not represent discrete genetic entities because they have been delimited artificially. Figure 1. The three morphological subsections of Antirrhinum. Nevertheless, support for the genetic distinction of some A representative of each subsection is shown in situ and in cultivation. Subsection Antirrhinum is represented by A. pseudomajus, subsection recognized species has been provided by allozymes and Streptosepalum is represented by A. braun-blanquetii and subsection Kick- DNA sequence variation (Mateu-Andres and Segarra- xiella is represented by A. pulverulentum. Scale bars: 150 mm for cultivated Moragues, 2000, 2003; Jimenez et al., 2005a; Mateu-Andres plants, and the ruler shown with plants in the field is 35 mm wide. and de Paco, 2005). Relationships above the species level are also unclear. The genus has been divided into three morphological subsections – Antirrhinum, Streptosepalum major subsections, and the involvement of many underlying and Kickxiella – but no subsection has been defined by a genes. However, all putative hybrid species appeared to synapomorphy, and all have been suggested to overlap in resemble one of their parents, suggesting that ancestral phenotype (Rothmaler, 1956; Webb, 1971). The subsections suites of phenotypes have survived hybridization as a result also correlate with ecology: most members of subsection of selection at multiple loci. Kickxiella are small prostrate alpines or xerophytes that grow on rock faces, whereas subsections Antirrhinum and RESULTS Streptosepalum comprise larger, more upright plants that Antirrhinum taxonomy reflects discontinuous phenotypic are able to grow in competition (Figure 1). This raises the variation possibility that each subsection represents an ecotype, and that its species have evolved similar characters indepen- Antirrhinum populations were sampled from across the dently as adaptations to a particular environment, rather geographic range of each recognized species and subspe- than sharing characters through common descent. cies, so that the depth of sampling in each taxon broadly Attempts to resolve a species phylogeny for Antirrhinum corresponded to its abundance (Figure 2; Tables 1 and S1). from DNA sequences have been unsuccessful. Relatively The only recognized species that remained un-sampled was little sequence variation has been found in the genus, Antirrhinum martenii, which could not be found at its ori- consistent with its recent origin, and the variation is not ginal collection sites in the Moroccan Rif. For convenience, distributed consistently between taxa, so that different we treated all taxa at the rank of species, including those that genes support different relationships between species are often regarded as subspecies of A. majus. (Jimenez et al., 2005b; Vargas et al., 2009). Sparse sampling To assess phenotypic variation within Antirrhinum we of the taxa used for DNA sequence analysis might also have grew plants from a representative subset of 98 populations contributed to a lack of phylogenetic resolution, given that together in a glasshouse, and recorded phenotypes for an young species are likely to share many unfixed alleles that average of 5.8 plants from each population (Table 2). We might not be represented in small taxon samples. chose phenotypes that differed between populations, with- Here, we examine evolutionary relationships within the out regard to their differences between species or sub- genus Antirrhinum by comparing populations sampled sections, to avoid any bias towards characters that might from across the geographic range of each species. Plastid automatically support traditional taxonomic divisions. Char- and multilocus nuclear genotypes resolve the relationships acters were then selected for further analysis on two genetic between many species, and further suggest that the tradi- criteria. The first attempted to reduce the use of characters tional morphological subsections largely correspond to that were strongly influenced by environment. It assumed separate evolutionary lineages. They also suggest that that members of the same species are genetically most hybridization has occurred repeatedly between the two similar to each other. Therefore, a comparison of the major ancestral lineages where they overlap in range. variation within species and between species gives an Morphometric analysis of plants grown in common garden estimate of the extent to which a phenotype is genetically conditions supported the phenotypic distinction of the two determined (approximating its broad-sense heritability). ª 2011 The Authors The Plant Journal ª 2011 Blackwell Publishing Ltd, The Plant Journal, (2011), 66, 1032–1043 1034 Yvette Wilson and Andrew Hudson Figure 2. The distribution of
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