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Molecular Ecology (2014) 23, 2137–2140 NEWS AND VIEWS PERSPECTIVE Go forth, evolve and prosper: the genetic basis of adaptive evolution in an invasive species S T E V E N J . F R A N K S * † and J A S O N MUNSHI-SOUTH*† *Department of Biological Sciences, Fordham University, 160 Larkin Hall, 441 E. Fordham Road, Bronx, NY 10458, USA; †Louis Calder Center-Biological Field Station, Fordham University, 53 Whippoorwill Road, Armonk, NY 10504, USA Invasive species stand accused of a familiar litany of offences, including displacing native species, disrupting ecological processes and causing billions of dollars in ecological damage (Cox 1999). Despite these transgressions, invasive species have at least one redeeming virtue – they offer us an unparalleled opportunity to investigate colonization and responses of populations to novel conditions in the invaded habitat (Elton 1958; Sakai et al. 2001). Invasive species are by definition colonists that have arrived and thrived in a new location. How they are able to thrive is of great interest, especially considering a paradox of invasion (Sax & Brown 2000): if many populations are locally adapted (Leimu & Fischer 2008), how could species introduced into new locations become so successful? One possibility is that populations adjust to the new conditions through plasticity – increasing production of allelopathic compounds (novel weapons), or taking advantage of new prey, for example. Alternatively, evolution could play a role, with the populations adapting to the novel conditions of the new habitat. There is increasing evidence, based on phenotypic data, for rapid adaptive evolution in invasive species (Franks et al. 2012; Colautti & Barrett 2013; Sultan et al. 2013). Prior studies have also demonstrated genetic changes in introduced populations using neutral markers, which generally do not provide information on adaptation. Thus, the genetic basis of adaptive evolution in invasive species has largely remained unknown. In this issue of Molecular Ecology, Vandepitte et al. (2014) provide some of the first evidence in invasive populations for molecular genetic changes directly linked to adaptation. Keywords: adaptation, flowering time genes, genomics, plant invasion, rapid evolution Correspondence: Steven J. Franks, Fax: 718-817-3645; E-mail: [email protected] © 2014 John Wiley & Sons Ltd Received 11 February 2014; revised 4 March 2014; accepted 8 March 2014 Vandepitte et al. (2014) studied Pyrenean rocket (Sisymbrium austriacum subsp. chrysanthum). This herbaceous plant is native to the Pyrenees mountains in Southern France and northern Spain and has recently invaded low elevation locations in Belgium and the Netherlands (Fig. 1A). The native and invaded ranges thus differ in several ecologically important factors such as elevation and latitude. The investigators also had a great resource for studying genetic changes during the process of colonization in this system: herbarium specimens of this species collected in the region between 1829 and 1955 (Fig. 1A). These herbarium collections allowed the investigators to document changes in allele frequencies over time (the most fundamental definition of evolution) rather than just inferring past changes based on current populations. This approach is part of a growing trend of using historical collections, including museum specimens (Hekkala et al. 2011; Rowe et al. 2011; Bi et al. 2013), samples from quarantine collections (Franks et al. 2011) and herbarium specimens (Martin et al. 2014) in population genetic studies. Pyrenean rocket also has the advantage of being in the Brassicaceae (crucifer or mustard) family (‘rocket’ is part of the common name of several crucifers). Thus, the researchers could take advantage of the wealth of genetic and genomic resources for the model plant Arabidopsis thaliana. Specifically, this study exemplifies how de novo SNP discovery for examining selection can be greatly enhanced by access to a high-quality, annotated reference genome from a related organism. Using one of the increasingly popular restriction-site-associated DNA sequencing (RAD-seq) methods (Narum et al. 2013), the authors first identified >15 000 SNPs from a pooled sample representing both invasive and native populations (Vandepitte et al. 2013) (Fig. 1B). However, many if not most SNPs identified by RAD-seq are unlikely to fall within protein-coding regions, and thus unlikely to be associated with functional processes through a relatively simple mechanism. To hone in on loci underlying traits potentially linked to adaptation to the invaded environment, the authors blasted their RADseq contigs against the Arabidopsis genome to identify SNPs within homologous genic regions. These SNPs were then further filtered by putative gene ontology annotations to identify likely candidates for functional variation in invaded populations. Taking advantage of another recently developed technique for cheap and rapid SNP genotyping (KASPar, i.e. genotyping by allele-specific amplification) (Fig. 1C), they validated the SNPs in a much broader sample of contemporary populations and herbarium specimens before identifying outlier loci exhibiting signatures of selection (Fig. 1D). Finally, the gene ontology annotations from 2138 N E W S A N D V I E W S : P E R S P E C T I V E (A) Source populations Introduced Herbarium (1825–1955) Native (B) RAD-Seq for (C) SNP genotyping SNP discovery (KASP) and validation G T G A T C T A C G T C (E) Gene ontology analysis FST (D) FST outlier analysis Photoperiodism, Other Location on chromosome Flowering Outlier SNPs (F) Change in SNP allele frequencies (evolution) Native Herbarium Introduced SNP 1 SNP 2 SNP 3 Fig. 1 Study overview. (A) The authors (Vandepitte et al. 2014) obtained tissue of Sisymbrium austriacum from three sources: the home range of the Pyrenees mountains in Southern France and northern Spain, the introduced range of Belgium and the Netherlands, and historical herbarium sheets collected between 1825 and 1955. (B) They used the genomic technique RAD-seq, with individuals from the home and introduced ranges only, to obtain SNPs (Vandepitte et al. 2013). (C) The competitive PCR-based technique KASP was used to genotype individuals from the home and introduced ranges and the historical herbarium specimens at 209 SNPs discovered by RAD-seq. (D) FST-outlier analysis was used to determine which SNPs were most genetically differentiated among all populations. These outliers are likely candidates for underlying traits related to environmental variation between the sites and evolutionary change over time. (E) The authors examined the putative function (gene ontology) of the outlier SNPs and compared the distribution of functions of outliers to that of all SNPs. The category of ‘photoperiodism/flowering time’ was significantly overrepresented in the outlier SNPs. (F) They examined allele frequencies at several outlier SNPs related to flowering time in historical herbarium specimens over time, current home range, current introduced range samples. They found allelic shifts at several flowering time loci, consistent with adaptive evolutionary change. © 2014 John Wiley & Sons Ltd N E W S A N D V I E W S : P E R S P E C T I V E 2139 the Arabidopsis genome were used to confirm that the outliers were enriched for a biologically meaningful class of processes (Fig. 1E). This set of approaches could be applied to a number of cases where a nonmodel study taxon is related to a species with a well-developed reference genome. The Vandepitte et al. (2014) study produced several important results. First, the study documented differences in allele frequencies between the native and introduced populations, as well as shifts in allele frequencies in the herbarium specimens over time (Fig. 1F). In several cases, the patterns match beautifully with expectations: for example, some alleles at low frequency in the native range gradually increased over time in the herbarium specimens and now occur at high frequency or are fixed in the introduced range. These changes in allele frequencies are definitive evidence for genetically based evolutionary change. Shifts in allele frequencies could be caused by selection or could be the result of neutral processes, such as genetic bottlenecks and founder effects, which could certainly occur in an introduced species. However, this study provides several lines of evidence that at least some of these allelic shifts are adaptive. First, several of the most highly differentiated SNPs, as determined by outlier FST analysis, are in genes known to influence flowering time. Also, the functional category of flowering time/photoperiod response was significantly overrepresented in the outlier SNPs. Although the authors did not provide data on phenotypic differences in flowering time or selection on flowering time between the native and invaded ranges, it seems reasonable that the optimal flowering time would differ between the home and introduced ranges, and that genes underlying this trait would be under selection in the invaded habitat. This result concurs with others that have found rapid adaptive shifts in plant phenology (Franks et al. 2007; Nevo et al. 2012; Colautti & Barrett 2013). Second, they found allele shifts at loci underlying these ecologically important traits, as expected with selection, rather than at random across the genome as expected with drift or a bottleneck. There was also no overall reduction in genetic diversity, indicating that the shifts in allele frequencies were likely not caused by founder events. There are several major implications of these findings. This work is part of a growing body of evidence that rapid evolution occurs and can be a key factor in understanding ecological processes and interactions (Pelletier et al. 2009). A recent book-length treatment of the subject identifies hundreds of such cases where the ‘. . .continual redeployment of standing genetic variation in different ways. . .’ has led to rapid evolution (Thompson 2013). This major shift in thinking about evolution contrasts with the expectations of Charles Darwin, who argued that evolution is an extremely slow process (Darwin 1859). The results not only indicate that evolution can occur rapidly, but also that the ability to rapidly adapt could be a key factor in explaining how invasive species are successful in novel conditions (Lee 2002; Colautti & Barrett 2013). Furthermore, the common ‘lag phase’ of invasion (Aikio et al. 2010) could be a © 2014 John Wiley & Sons Ltd direct result of species first adapting to new conditions and then rapidly expanding their population sizes and ranges. The results of this study also inform a major question about the genetic basis of evolutionary change, which is to what degree selection acts on standing genetic variation vs. rare alleles or new mutations. Here, the authors found that all alleles in the invading population were present in the native population, indicating that selection acted on existing variation rather than very rare alleles or new mutations. As a snapshot of a contemporary evolutionary event, this work is a convincing case study of the genetic basis of rapid adaptive evolution through colonization that is relevant for understanding the processes of local adaptation and adaptive radiation. 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