Download Go forth, evolve and prosper: the genetic basis of adaptive evolution

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. Future studies should address
other cases where native species have been forced to adapt
to human alteration of the environment, such as pollution
(Bashalkhanov et al. 2013), urbanization (Harris et al. 2013)
and climate change (Manel et al. 2012).
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doi: 10.1111/mec.12718
© 2014 John Wiley & Sons Ltd