Introduction
Most organisms exhibit plastic responses to the developmental
environment. These responses are adaptive if they generate phenotypes
suited to conditions in spatially and/or temporally heterogeneous
habitats (Lande 2009, Monaghan 2008, Arnold et al. 2019). Indeed,
developmental plasticity (i.e., the capacity of a genotype to express
multiple phenotypes in response to early-life environments) is one route
by which organisms could overcome the challenges of environmental
heterogeneity (West-Eberhard 2003, DeWitt and Scheiner 2004; Snell-Rood
and Ehlman 2021). For example, some species develop defensive
morphologies when predators are detected, but otherwise, do not expend
energy on these traits (e.g. Daphnia waterfleas, Parejko and
Dodson 1991; larval amphibians, Newman 1989). Such plasticity is
described by a reaction norm, which is a mathematical function that
describes phenotype values across different environments. Consequently,
reaction norms are useful tools to calculate, visualize, and evaluate
differences in plastic traits among environments, populations, and
individuals (Gomulkiewicz and Kirkpatrick 1992, Brommer et al. 2005,
Monaghan 2008).
Reaction norms may vary among individuals and populations, potentially
due to genetic variation (Ellis and Boyce 2008; Scheiner 1993, Murren et
al. 2015). This indicates an opportunity for natural selection to shape
plasticity in adaptive ways (Levis and Pfenning 2016) like any trait
with additive genetic variation (Hillesheim and Stearns 1991, Gavrilets
and Scheiner 1993, Scheiner 2002). Environmental heterogeneity creates
conditions that allow developmental plasticity to be adaptive
(Gomulkiewicz and Kirkpatrick 1992, Lande 2009), as selection will favor
reaction norms that match phenotypes to different environments, thereby
enhancing fitness. Furthermore, adaptive plasticity should arise if the
environmental cues that generate a phenotype also predict the future
environment in which the phenotype is expressed and where its fitness
consequences are realized (Casal et al. 2004, Beldade et al 2011).
Variation in reaction norms among individuals of a population provides
an opportunity for selection to act on plasticity, whereas variation
across populations may signify past selection that has shaped plasticity
in response to local environments. Both theory (Gavrilets and Scheiner
1993; Lande 2009, Levis and Pfenning 2016) and empirical studies (Suzuki
and Nijhout 2006) indicate that under strong selection, the magnitude
(i.e., slope) of reaction norms should be maintained and become
homogenized, decreasing within-population variation. Alternatively, if
distinct populations experience different environmental pressures with
varying levels of heterogeneity, then both the magnitude and variation
of reaction norms might change (Duffy et al. 2015). Moreover,
experimental evolution studies demonstrate that patterns of plasticity
can vary between populations (e.g., populations with or without
plasticity; van der Burg et al. 2020), and this process could be
reversed with artificial or natural selection. Ultimately, a
population’s genetic structure may contain individuals that are more (or
less) plastic to environmental conditions. Consequently, when a
population is faced with a major environmental change due to natural or
human-induced causes, or resulting from invasion, plasticity may be
amenable to selection.
The aim of this study is to quantify variation in developmental reaction
norms among individuals and within populations of a non-native lizard,
the brown anole (Anolis sagrei ). Past work on A. sagrei (Warner et al. 2012; Pearson & Warner 2018; Hall & Warner 2022), as
well as studies on other reptiles (Mitchell et al. 2018; Noble et al.
2018; Warner et al. 2018), demonstrate strong effects of egg incubation
environments on developmental rate, offspring body size, locomotor
performance, behavior, physiology, and fitness; however, within- and
among-population variation in reaction norms has never been examined inA. sagrei , but among-population variation in embryonic reaction
norms of other Anolis species has been documented (Goodman 2008;
Goodman & Heah 2010). Here, we collected lizards from two islands that
differ in habitat structure and, thus, the predominant nest environments
in which embryos develop (i.e., open-canopy island with warm, dry
conditions versus closed-canopy with cool, moist conditions).
Individuals from each island were bred in a common garden, and we
incubated eggs in one of two regimes that mimic natural conditions on
each island. Because each females’ eggs were divided between treatments
(i.e., split-clutch design), we could quantify among-individual and
among-population variation in reaction norms for a range of
fitness-related phenotypes.
Our novel study design helps fill two important knowledge gaps in
studies of developmental plasticity. First, most studies of
developmental plasticity consider the isolated effects of factors like
incubation temperature or moisture, but such factors usually co-vary in
predictable ways in the wild (e.g. warmer nests are often drier; Pruett
et al. 2020). We need a better understanding of the effects of real nest
environments on plasticity. For example, warmer temperatures result in
greater sprint speed at hatching (Pearson & Warner 2018), but dry
incubation conditions can decrease hatchling performance (Gatto & Reina
2022). Moreover, the effect of temperature on sprint speed may depend
upon thermal variation, not just mean temperature (Hall & Warner 2020).
Thus, we need studies that combine multiple nest conditions that
represent real habitats to better understand developmental plasticity in
the wild.
Second, we test the hypothesis that variation in offspring phenotypes
results from the influence of the environment (i.e., open- vs
closed-canopy conditions), parentally induced variation in phenotypes
(i.e., family-group reaction norm intercepts), and plasticity (i.e.,
family-group reaction norm slopes). We address this hypothesis by
quantifying the slopes of reaction norms (for morphological,
physiological, and performance traits) for each family group and
comparing them among families and populations. Significant variation in
reaction norm slopes among family groups (indicative of genetic x
environment interactions) would support this hypothesis and indicate
potential for plasticity to evolve in response to future pressures. Our
results have important implications for understanding how natural
developmental environments generate phenotypic variation, and the
capacity for populations to adapt to changing environments.