Introduction
Biological invasions enable researchers to conduct studies at large
spatial and temporal scales that capture substantial environmental
variation, facilitating the ability to observe ecological and
evolutionary processes over contemporary timescales (Sakai et al., 2001;
Sax et al., 2007; Lawson et al., 2011; Hodgins et al., 2018). When
non-native populations encounter new environments in terms of predators,
competitors, or abiotic conditions, this variation can relax selection
experienced in their native range and/or impose novel selective
pressures (Sakai et al., 2001; Lee, 2002; Bock et al., 2015, 2021).
Invasions have provided many recent examples of rapid adaptation (e.g.,
Colautti & Barrett, 2013; Stern & Lee, 2020; Battlay et al., 2023).
Previous studies have demonstrated phenotypic shifts in non-native
species driven by natural selection occurring over the course of tens to
hundreds of generations (e.g., Huey et al., 2000; Shine, 2011; Colautti
& Barrett, 2013; Bock et al., 2018). Yet not all invasions result in
rapid adaptation, even when non-native populations experience novel
environments, due to a variety of factors such as a lack of associated
selective pressures, little relevant genetic variation, or possible
genetic constraints (e.g., Alexander & Edwards, 2010; Bock et al.,
2021, Baeckens et al., 2023, Bock et al., 2023).
In addition to examples of rapid adaptation, studies of biological
invasions have revealed the importance of the invasion history for
patterns of demographic, genetic and phenotypic variation (e.g., Kolbe
et al., 2004; Cristescu, 2015). I
nvasion history includes the contribution to genetic ancestry through
the location and number of source populations in the native range (Kolbe
et al., 2004, 2007a), the spread of populations in the non-native range
(e.g., leading to ‘expansion load’; Peischl et al., 2013), and the
extent of admixture (i.e., intraspecific hybridization of previously
isolated sources) within non-native populations (Rius & Darling, 2014;
Bock et al., 2021), among other factors. As a result, genetic and
phenotypic variation can increase or decrease in invasive populations
during an invasion. For example, admixture will often increase variation
(Kolbe et al., 2004, 2008; Rius & Darling, 2014), whereas random
genetic drift will decrease variation through founder effects and
population bottlenecks (Dlugosch & Parker, 2008; Ficetola et al., 2008;
Zhu et al., 2017). The invasion history is expected to have a strong
effect on patterns of genetic and phenotypic variation within and among
non-native populations, and can strongly bias the interpretation of
drivers of evolution during invasions, when not properly accounted for
(Keller & Taylor, 2008; Colautti et al., 2009; Hodgins et al., 2018).
Therefore, understanding evolution in introduced populations will often
require elucidating the combined effects of invasion history and
adaptation to environmental conditions encountered in the novel range.
The biological invasion of the brown anole lizard (Anolis sagrei )
provides an excellent opportunity to test hypotheses for phenotypic
evolution among non-native populations. Native to the northern
Caribbean—Cuba, Bahamas, Cayman Brac and Little Cayman—the brown
anole is a very successful invasive lizard that has been repeatedly
introduced to Florida (USA) starting in the late 19th century (Garman,
1887) and expanding rapidly beginning in 1950s (Campbell, 1996). At
least eight introduction events from genetically distinct native-range
populations have resulted in non-native populations with greater genetic
diversity than those observed in the native range (Kolbe et al., 2004,
2007a, 2008; Bock et al., 2021). Also, non-native Florida populations
are more morphologically variable in body size and shape, number of
toepad lamellae, and number of scales compared to native Cuban
populations (Lee, 1992; Kolbe et al., 2007a). This increased phenotypic
and genetic variation may be acted upon by natural selection, which
could promote evolution and facilitate invasion success (e.g., Shine
2011, but see Jaspers et al., 2021). Introduced populations differ
significantly from each other in genetic variation and certain
morphological traits (Kolbe et al., 2007a, 2008; Bock et al., 2021).
Thus, the invasion history may dominate patterns of phenotypic and
genetic variation in these non-native populations. Indeed, genetic
ancestry rather than local adaptation better explains variation among
non-native brown anole populations in morphology and water loss traits
(Kolbe et al., 2007a; Bock et al., 2021; Baeckens et al., 2023).
Moreover, novel genetic interactions that result from hybridization
(e.g., Bock et al., 2021) and high linkage disequilibrium in chromosomal
segments of reduced recombination (i.e., Bock et al., 2023) may play a
role in constraining adaptive responses in the invasive range.
Given the lack of previous evidence for local adaptation among
non-native brown anole populations, we wanted to focus on a
phenotypically and genetically complex trait that is subject of multiple
selective pressures to increase the chance of detecting evidence of
natural selection.
We therefore examined evolutionary change across the invasive range in
the iconic Anolis signaling ornament: the dewlap. Dewlaps are
extendable structures located on the throat of anoles that differ in
size, shape, color, and patterning at both the inter- and intraspecific
levels (Losos, 2009). This multifaceted signaling structure often plays
an important role in territory establishment and defense (e.g.,
Fleishman, 1992), reproductive interactions (e.g., Crews, 1975), species
recognition (e.g., Rand & Williams, 1970; Losos, 1985), and predator
deterrence (e.g., Leal & Rodríguez-Robles, 1995; Leal &
Rodríguez-Robles, 1997a,b). Considerable evidence supports that the
dewlap is subject to a variety of selection pressures (Leal &
Fleishman, 2002, 2004; Vanhooydonck et al., 2009; Ng et al., 2013a;
Driessens et al., 2017). Previous research has shown strong, albeit
contrasting, relationships between environmental conditions and dewlap
design in native populations of Anolis lizards (Leal and
Fleishman, 2002, 2004; Ng et al., 2013a; see Discussion for details).
For brown anoles, native-range populations inhabiting mesic environments
had primarily marginal dewlaps (i.e., red or orange covering most of the
dewlap with yellow along the outer margin), showing high reflectance in
red, whereas lizards occupying xeric environments had a higher
proportion of solid dewlaps with higher ultraviolet (UV) reflectance
(Driessens et al., 2017).
These results show that Anolis dewlap phenotypes are associated
with variation in environmental conditions, likely resulting from
differential selection on signal effectiveness in response to climatic
conditions and physical habitat characteristics (Endler, 1992, 1993) as
well as interactions with competitors, predators, and conspecifics
(Cole, 2013).
In this study, we investigated multiple aspects of a complex trait in
brown anole populations across a large portion of its non-native range
in the southeastern United States. Our goal was to determine whether
among-population variation in aspects of dewlap design can be best
explained by environmental conditions (consistent with local
adaptation), genetic ancestry, or a combination of both factors.
Specifically, we tested whether variation in dewlap characteristics
(i.e., color, pattern and size) were associated with 1) differences in
prevailing environmental conditions (i.e., temperature, precipitation,
and light conditions) and 2) genetic ancestry as measured by the
relative contribution of genome-wide SNP variation inherited from
different native-range source populations (Kolbe et al., 2004, 2007a,
2008, Bock et al., 2021). We complemented the latter ancestry-based
tests with genome-wide trait association analyses, taking advantage of
recent analytical developments that allow ancestry-specific associations
to be detected along the genome (e.g., Skotte et al., 2019). Further, we
relied on F ST outlier analyses and
genotype-environment association analyses, which can identify loci
involved in adaptation. The phenotypically diverse and putatively
polygenic nature of complex traits, such as the Anolis dewlap,
afford an excellent opportunity to assess whether changing environmental
conditions during an invasion shape phenotypic variation in ways
consistent with natural selection. The brown anole invasion is a
particularly useful case because previous studies of morphological and
physiological traits have failed to provide evidence of adaptation
during the invasion (i.e., Kolbe et al., 2007a, Bock et al., 2021,
Baeckens et al., 2023, Bock et al., 2023). A better understanding of the
evolutionary dynamics during biological invasions is useful for
predicting future impacts of invasive species, especially as global
environments continue to change rapidly.