Phenotypic integration plasticity in Daphnia magna: an integral facet of G × E interactions

Phenotypic integration can be defined as the network of multivariate relationships among behavioural, physiological and morphological traits that describe the organism. Phenotypic integration plasticity refers to the change in patterns of phenotypic integration across environments or ontogeny. Because studies of phenotypic plasticity have predominantly focussed on single traits, a G × E interaction is typically perceived as differences in the magnitude of trait expression across two or more environments. However, many plastic responses involve coordinated responses in multiple traits, raising the possibility that relative differences in trait expression in different environments are an important, but often overlooked, source of G × E interaction. Here, we use phenotypic change vectors to statistically compare the multivariate life‐history plasticity of six Daphnia magna clones collected from four disparate European populations. Differences in the magnitude of plastic responses were statistically distinguishable for two of the six clones studied. However, differences in phenotypic integration plasticity were statistically distinguishable for all six of the clones studied, suggesting that phenotypic integration plasticity is an important component of G × E interactions that may be missed unless appropriate multivariate analyses are used.     

Rapid evolution in response to introduced predators II: the contribution of adaptive plasticity

Background  

Introductions of non-native species can significantly alter the selective environment for populations of native species, which can respond through phenotypic plasticity or genetic adaptation. We examined phenotypic and genetic responses of Daphnia populations to recent introductions of non-native fish to assess the relative roles of phenotypic plasticity versus genetic change in causing the observed patterns. The Daphnia community in alpine lakes throughout the Sierra Nevada of California (USA) is ideally suited for investigation of rapid adaptive evolution because there are multiple lakes with and without introduced fish predators. We conducted common-garden experiments involving presence or absence of chemical cues produced by fish and measured morphological and life-history traits in Daphnia melanica populations collected from lakes with contrasting fish stocking histories. The experiment allowed us to assess the degree of population differentiation due to fish predation and examine the contribution of adaptive plasticity in the response to predator introduction.     

Brain size predicts behavioural plasticity in guppies (Poecilia reticulata): An experiment

Understanding how animal personality (consistent between‐individual behavioural differences) arises has become a central topic in behavioural sciences. This endeavour is complicated by the fact that not only the mean behaviour of individuals (behavioural type) but also the strength of their reaction to environmental change (behavioural plasticity) varies consistently. Personality and cognitive abilities are linked, and we suggest that behavioural plasticity could also be explained by differences in brain size (a proxy for cognitive abilities), since accurate decisions are likely essential to make behavioural plasticity beneficial. We test this idea in guppies (Poecilia reticulata), artificially selected for large and small brain size, which show clear cognitive differences between selection lines. To test whether those lines differed in behavioural plasticity, we reared them in groups in structurally enriched environments and then placed adults individually into empty tanks, where we presented them daily with visual predator cues and monitored their behaviour for 20 days with video‐aided motion tracking. We found that individuals differed consistently in activity and risk‐taking, as well as in behavioural plasticity. In activity, only the large‐brained lines demonstrated habituation (increased activity) to the new environment, whereas in risk‐taking, we found sensitization (decreased risk‐taking) in both brain size lines. We conclude that brain size, potentially via increasing cognitive abilities, may increase behavioural plasticity, which in turn can improve habituation to novel environments. However, the effects seem to be behaviour‐specific. Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level.     

A Continuum of Behavioral Plasticity in Urban and Desert Black Widows

Behavioral plasticity marks an individual's ability to modulate behavior across functional contexts. Behavioral syndromes, on the other hand, appear as consistent individual variation in behavior that is both repeatable for individuals within a functional context (e.g., consistent voracity toward prey) and correlated across contexts (e.g., high voracity toward prey and high levels of boldness toward enemies). Thus, adaptive plasticity and syndromes represent two extremes of a behavioral plasticity continuum upon which most behavioral phenotypes fall. We tested for both adaptive plasticity and behavioral syndromes in the western black widow spider, Latrodectus hesperus. We measured behavior in three contexts: startle, startle + prey, and startle + mate, and found (1) classic behaviorally plastic responses to predation risk, (2) high repeatability of behavior within contexts, and (3) evidence of a correlation between startle + prey and startle + mate contexts, indicative of a behavioral syndrome. As relative behavioral plasticity may vary across populations, we also compared urban and desert populations to test whether spiders from these habitats exhibit different behaviors and/or behavioral syndromes. While we found that urban males used in mating trials courted urban females significantly more than desert females, we found no other differences in the behavior of urban and desert black widows. Thus, black widows, regardless of habitat, are characterized by both context‐specific behavioral plasticity and across‐context correlations, presenting a phenotypic complexity that is likely exhibited, to varying degrees, by most organisms.     

The role of phenotypic plasticity in driving genetic evolution

Models of population divergence and speciation are often based on the assumption that differences between populations are due to genetic factors, and that phenotypic change is due to natural selection. It is equally plausible that some of the differences among populations are due to phenotypic plasticity. We use the metaphor of the adaptive landscape to review the role of phenotypic plasticity in driving genetic evolution. Moderate levels of phenotypic plasticity are optimal in permitting population survival in a new environment and in bringing populations into the realm of attraction of an adaptive peak. High levels of plasticity may increase the probability of population persistence but reduce the likelihood of genetic change, because the plastic response itself places the population close to a peak. Moderate levels of plasticity arise whenever multiple traits, some of which are plastic and others not, form a composite trait involved in the adaptive response. For example, altered behaviours may drive selection on morphology and physiology. Because there is likely to be a considerable element of chance in which behaviours become established, behavioural change followed by morphological and physiological evolution may be a potent force in driving evolution in novel directions. We assess the role of phenotypic plasticity in stimulating evolution by considering two examples from birds: (i) the evolution of red and yellow plumage coloration due to carotenoid consumption; and (ii) the evolution of foraging behaviours on islands. Phenotypic plasticity is widespread in nature and may speed up, slow down, or have little effect on evolutionary change. Moderate levels of plasticity may often facilitate genetic evolution but careful analyses of individual cases are needed to ascertain whether plasticity has been essential or merely incidental to population differentiation.     

Thermal adaptation and phenotypic plasticity in a warming world: Insights from common garden experiments on Alaskan sockeye salmon

An important unresolved question is how populations of coldwater‐dependent fishes will respond to rapidly warming water temperatures. For example, the culturally and economically important group, Pacific salmon (Oncorhynchus spp.), experience site‐specific thermal regimes during early development that could be disrupted by warming. To test for thermal local adaptation and heritable phenotypic plasticity in Pacific salmon embryos, we measured the developmental rate, survival, and body size at hatching in two populations of sockeye salmon (Oncorhynchus nerka) that overlap in timing of spawning but incubate in contrasting natural thermal regimes. Using a split half‐sibling design, we exposed embryos of 10 families from each of two populations to variable and constant thermal regimes. These represented both experienced temperatures by each population, and predicted temperatures under plausible future conditions based on a warming scenario from the downscaled global climate model (MIROC A1B scenario). We did not find evidence of thermal local adaptation during the embryonic stage for developmental rate or survival. Within treatments, populations hatched within 1 day of each other, on average, and among treatments, did not differ in survival in response to temperature. We did detect plasticity to temperature; embryos developed 2.5 times longer (189 days) in the coolest regime compared to the warmest regime (74 days). We also detected variation in developmental rates among families within and among temperature regimes, indicating heritable plasticity. Families exhibited a strong positive relationship between thermal variability and phenotypic variability in developmental rate but body length and mass at hatching were largely insensitive to temperature. Overall, our results indicated a lack of thermal local adaptation, but a presence of plasticity in populations experiencing contrasting conditions, as well as family‐specific heritable plasticity that could facilitate adaptive change.     

Phenotypic plasticity alone cannot explain climate‐induced change in avian migration timing

Recent climate change has been linked to shifts in the timing of life-cycle events in many organisms, but there is debate over the degree to which phenological changes are caused by evolved genetic responses of populations or by phenotypic plasticity of individuals. We estimated plasticity of spring arrival date in 27 species of bird that breed in the vicinity of an observatory in eastern North America. For 2441 individuals detected in multiple years, arrival occurred earlier during warm years, especially in species that migrate short distances. Phenotypic plasticity averaged −0.93 days °C⁻¹ ± 0.70 (95% CI). However, plasticity accounted for only 13–25% of the climate-induced trend in phenology observed over 46 years. Although our approach probably underestimates the full scope of plasticity, the data suggest that part of the response to environmental change has been caused by microevolution. The estimated evolutionary rates are plausible (0.016 haldanes).     

Plasticity in functional traits in the context of climate change: a case study of the subalpine forb Boechera stricta (Brassicaceae)

Environmental variation often induces shifts in functional traits, yet we know little about whether plasticity will reduce extinction risks under climate change. As climate change proceeds, phenotypic plasticity could enable species with limited dispersal capacity to persist in situ, and migrating populations of other species to establish in new sites at higher elevations or latitudes. Alternatively, climate change could induce maladaptive plasticity, reducing fitness, and potentially stalling adaptation and migration. Here, we quantified plasticity in life history, foliar morphology, and ecophysiology in Boechera stricta (Brassicaceae), a perennial forb native to the Rocky Mountains. In this region, warming winters are reducing snowpack and warming springs are advancing the timing of snow melt. We hypothesized that traits that were historically advantageous in hot and dry, low‐elevation locations will be favored at higher elevation sites due to climate change. To test this hypothesis, we quantified trait variation in natural populations across an elevational gradient. We then estimated plasticity and genetic variation in common gardens at two elevations. Finally, we tested whether climatic manipulations induce plasticity, with the prediction that plants exposed to early snow removal would resemble individuals from lower elevation populations. In natural populations, foliar morphology and ecophysiology varied with elevation in the predicted directions. In the common gardens, trait plasticity was generally concordant with phenotypic clines from the natural populations. Experimental snow removal advanced flowering phenology by 7 days, which is similar in magnitude to flowering time shifts over 2–3 decades of climate change. Therefore, snow manipulations in this system can be used to predict eco‐evolutionary responses to global change. Snow removal also altered foliar morphology, but in unexpected ways. Extensive plasticity could buffer against immediate fitness declines due to changing climates.     

Seasonal and diel plasticity of song type use in individual ovenbirds (Seiurus aurocapilla)

Animal communication is an important aspect of ecology across taxa, and there is a growing area of research that examines how animals plastically adjust their signals to account for both abiotic and biotic factors. Song type use and the temporal plasticity of song have been described in many bird species, but as of yet, few studies have examined how song type use may change across both seasonal and diel timeframes, and no studies have considered individual-level variation in plasticity. Using a hierarchical framework, we examined temporal patterns of primary and flight song use in ovenbirds (Seiurus aurocapilla; N = 21 individuals). We recorded ovenbird songs (N = 99,259) with autonomous recorders over 24-hr periods once per week across a breeding season near Sault Ste. Marie, Canada. As predicted, the occurrence and frequency of both song types significantly decreased over the season and showed temporal separation over diel periods. Primary songs peaked at dawn and declined throughout the day, while flight songs peaked at dusk and night. Our results support that primary songs have multiple functions as they remained more frequent during dawn and morning across the breeding season, while flight songs likely serve an intersexual function as they decreased similarly for all diel periods as mating opportunities decreased. Individuals were consistent in how frequently they sang their primary songs, but not their flight songs, suggesting that flight songs are more plastically expressed. We highlight the importance of examining plasticity in animal communication at the individual level as we show that males significantly differed in both their song behaviours (random intercepts) and the seasonal plasticity (random slopes) in these behaviours. Integrating themes such as song type use, temporal plasticity, and individual variation will be important for examining the evolutionary mechanisms that shape animal communication systems.     

Thermal tolerance in the keystone species Daphnia magna—a candidate gene and an outlier analysis approach

Changes in temperature have occurred throughout Earth's history. However, current warming trends exacerbated by human activities impose severe and rapid loss of biodiversity. Although understanding the mechanisms orchestrating organismal response to climate change is important, remarkably few studies document their role in nature. This is because only few systems enable the combined analysis of genetic and plastic responses to environmental change over long time spans. Here, we characterize genetic and plastic responses to temperature increase in the aquatic keystone grazer Daphnia magna combining a candidate gene and an outlier analysis approach. We capitalize on the short generation time of our species, facilitating experimental evolution, and the production of dormant eggs enabling the analysis of long‐term response to environmental change through a resurrection ecology approach. We quantify plasticity in the expression of 35 candidate genes in D. magna populations resurrected from a lake that experienced changes in average temperature over the past century and from experimental populations differing in thermal tolerance isolated from a selection experiment. By measuring expression in multiple genotypes from each of these populations in control and heat treatments, we assess plastic responses to extreme temperature events. By measuring evolutionary changes in gene expression between warm‐ and cold‐adapted populations, we assess evolutionary response to temperature changes. Evolutionary response to temperature increase is also assessed via an outlier analysis using EST‐linked microsatellite loci. This study provides the first insights into the role of plasticity and genetic adaptation in orchestrating adaptive responses to environmental change in D. magna.     

Context is key: A comment on Herczeg et al. 2019

In the last several years, there has been a surge in the number of studies addressing the causes and consequences of among‐individual variation in cognitive ability and behavioural plasticity. Here, we use a recent publication by Herczeg et al. (2019: 32(3), 218–226) to highlight three shortcomings common to this newly emerging field. In their study, Herczeg et al. attempted to link variation in cognitive ability and behavioural plasticity by testing whether selection lines of guppies (Poecilia reticulata) that differ in relative brain size also differ in behavioural plasticity, as might be expected if the costs to plasticity are predominantly derived from the cost of developing large brains. First, residual brain size may not be a suitable proxy for ‘cognitive ability’. Recent work has shown that intraspecific variation in cognitive ability can be better understood by considering variation in the specific brain areas responsible for the relevant behaviours as opposed to whole‐brain mass. Second, the measure of behavioural plasticity, habituation, is unlikely to fulfil the assumptions that plasticity is both adaptive and costly. Finally, we point out several misconceptions regarding animal personality that continue to contribute to the choice of traits that are not well aligned with study objectives. Elucidating the mechanisms underlying among‐individual variation in cognition and behavioural plasticity within populations requires integration between behavioural ecology and comparative cognition, and the study system developed by Herczeg et al. has the potential to provide important mechanistic insights. We hope that by articulating and critically appraising the underlying assumptions that are common in these traditionally separate disciplines, a strong foundation can emerge to allow for more fruitful integration of these fields.     

Will phenotypic plasticity affecting flowering phenology keep pace with climate change?

Rising temperatures have begun to shift flowering time, but it is unclear whether phenotypic plasticity can accommodate projected temperature change for this century. Evaluating clines in phenological traits and the extent and variation in plasticity can provide key information on assessing risk of maladaptation and developing strategies to mitigate climate change. In this study, flower phenology was examined in 52 populations of big sagebrush (Artemisia tridentata) growing in three common gardens. Flowering date (anthesis) varied 91 days from late July to late November among gardens. Mixed‐effects modeling explained 79% of variation in flowering date, of which 46% could be assigned to plasticity and genetic variation in plasticity and 33% to genetics (conditional R² = 0.79, marginal R² = 0.33). Two environmental variables that explained the genetic variation were photoperiod and the onset of spring, the Julian date of accumulating degree‐days >5 °C reaching 100. The genetic variation was mapped for contemporary and future climates (decades 2060 and 2090), showing flower date change varies considerably across the landscape. Plasticity was estimated to accommodate, on average, a ±13‐day change in flowering date. However, the examination of genetic variation in plasticity suggests that the magnitude of plasticity could be affected by variation in the sensitivity to photoperiod and temperature. In a warmer common garden, lower‐latitude populations have greater plasticity (+16 days) compared to higher‐latitude populations (+10 days). Mapped climatypes of flowering date for contemporary and future climates illustrate the wide breadth of plasticity and large geographic overlap. Our research highlights the importance of integrating information on genetic variation, phenotypic plasticity and climatic niche modeling to evaluate plant responses and elucidate vulnerabilities to climate change.     

Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

• Plants are part of biodiverse communities and frequently suffer from attack by multiple herbivorous insects. Plant responses to these herbivores are specific for insect feeding guilds: aphids and caterpillars induce different plant phenotypes. Moreover, plants respond differentially to single or dual herbivory, which may cascade into a chain of interactions in terms of resistance to other community members. Whether differential responses to single or dual herbivory have consequences for plant resistance to yet a third herbivore is unknown.
• We assessed the effects of single or dual herbivory by Brevicoryne brassicae aphids and/or Plutella xylostella caterpillars on resistance of plants from three natural populations of wild cabbage to feeding by caterpillars of Mamestra brassicae. We measured plant gene expression and phytohormone concentrations to illustrate mechanisms involved in induced responses.
• Performance of both B. brassicae and P. xylostella was reduced when feeding simultaneously with the other herbivore, compared to feeding alone. Gene expression and phytohormone concentrations in plants exposed to dual herbivory were different from those found in plants exposed to herbivory by either insect alone. Plants previously induced by both P. xylostella and B. brassicae negatively affected growth of the subsequently arriving M. brassicae. Furthermore, induced responses varied between wild cabbage populations.
• Feeding by multiple herbivores differentially activates plant defences, which has plant‐mediated negative consequences for a subsequently arriving herbivore. Plant population‐specific responses suggest that plant populations adapt to the specific communities of insect herbivores. Our study contributes to the understanding of plant defence plasticity in response to multiple insect attacks.

     

Clinal adaptation and adaptive plasticity in Artemisia californica: implications for the response of a foundation species to predicted climate change

Local adaptation and plasticity pose significant obstacles to predicting plant responses to future climates. Although local adaptation and plasticity in plant functional traits have been documented for many species, less is known about population‐level variation in plasticity and whether such variation is driven by adaptation to environmental variation. We examined clinal variation in traits and performance – and plastic responses to environmental change – for the shrub Artemisia californica along a 700 km gradient characterized (from south to north) by a fourfold increase in precipitation and a 61% decrease in interannual precipitation variation. Plants cloned from five populations along this gradient were grown for 3 years in treatments approximating the precipitation regimes of the north and south range margins. Most traits varying among populations did so clinally; northern populations (vs. southern) had higher water‐use efficiencies and lower growth rates, C : N ratios and terpene concentrations. Notably, there was variation in plasticity for plant performance that was strongly correlated with source site interannual precipitation variability. The high‐precipitation treatment (vs. low) increased growth and flower production more for plants from southern populations (181% and 279%, respectively) than northern populations (47% and 20%, respectively). Overall, precipitation variability at population source sites predicted 86% and 99% of variation in plasticity in growth and flowering, respectively. These striking, clinal patterns in plant traits and plasticity are indicative of adaptation to both the mean and variability of environmental conditions. Furthermore, our analysis of long‐term coastal climate data in turn indicates an increase in interannual precipitation variation consistent with most global change models and, unexpectedly, this increased variation is especially pronounced at historically stable, northern sites. Our findings demonstrate the critical need to integrate fundamental evolutionary processes into global change models, as contemporary patterns of adaptation to environmental clines will mediate future plant responses to projected climate change.     

Structural Plasticity Can Produce Metaplasticity

Background

Synaptic plasticity underlies many aspect of learning memory and development. The properties of synaptic plasticity can change as a function of previous plasticity and previous activation of synapses, a phenomenon called metaplasticity. Synaptic plasticity not only changes the functional connectivity between neurons but in some cases produces a structural change in synaptic spines; a change thought to form a basis for this observed plasticity. Here we examine to what extent structural plasticity of spines can be a cause for metaplasticity. This study is motivated by the observation that structural changes in spines are likely to affect the calcium dynamics in spines. Since calcium dynamics determine the sign and magnitude of synaptic plasticity, it is likely that structural plasticity will alter the properties of synaptic plasticity.

Methodology/Principal Findings

In this study we address the question how spine geometry and alterations of N-methyl-D-aspartic acid (NMDA) receptors conductance may affect plasticity. Based on a simplified model of the spine in combination with a calcium-dependent plasticity rule, we demonstrated that after the induction phase of plasticity a shift of the long term potentiation (LTP) or long term depression (LTD) threshold takes place. This induces a refractory period for further LTP induction and promotes depotentiation as observed experimentally. That resembles the BCM metaplasticity rule but specific for the individual synapse. In the second phase, alteration of the NMDA response may bring the synapse to a state such that further synaptic weight alterations are feasible. We show that if the enhancement of the NMDA response is proportional to the area of the post synaptic density (PSD) the plasticity curves most likely return to the initial state.

Conclusions/Significance

Using simulations of calcium dynamics in synaptic spines, coupled with a biophysically motivated calcium-dependent plasticity rule, we find under what conditions structural plasticity can form the basis of synapse specific metaplasticity.     

Does thermal plasticity align with local adaptation? An interspecific comparison of wing morphology in sepsid flies

Although genetic and plastic responses are sometimes considered as unrelated processes, their phenotypic effects may often align because genetic adaptation is expected to mirror phenotypic plasticity if adaptive, but run counter to it when maladaptive. Because the magnitude and direction of this alignment has further consequences for both the tempo and mode of adaptation, they are relevant for predicting an organisms’ reaction to environmental change. To better understand the interplay between phenotypic plasticity and genetic change in mediating adaptive phenotypic variation to climate variability, we here quantified genetic latitudinal variation and thermal plasticity in wing loading and wing shape in two closely related and widespread sepsid flies. Common garden rearing of 16 geographical populations reared across multiple temperatures revealed that wing loading decreases with latitude in both species. This pattern could be driven by selection for increased dispersal capacity in the cold. However, although allometry, sexual dimorphism, thermal plasticity and latitudinal differentiation in wing shape all show similar patterns in the two species, the relationship between the plastic and genetic responses differed between them. Although latitudinal differentiation (south to north) mirrored thermal plasticity (hot to cold) in Sepsis punctum, there was no relationship in Sepsis fulgens. While this suggests that thermal plasticity may have helped to mediate local adaptation in S. punctum, it also demonstrates that genetic wing shape differentiation and its relation to thermal plasticity may be complex and idiosyncratic, even among ecologically similar and closely related species. Hence, genetic responses can, but do not necessarily, align with phenotypic plasticity induced by changing environmental selection pressures.     

Sustainable harvest: managing plasticity for resilient crops

Maintaining crop production to feed a growing world population is a major challenge for this period of rapid global climate change. No consistent conceptual or experimental framework for crop plants integrates information at the levels of genome regulation, metabolism, physiology and response to growing environment. An important role for plasticity in plants is assisting in homeostasis in response to variable environmental conditions. Here, we outline how plant plasticity is facilitated by epigenetic processes that modulate chromatin through dynamic changes in DNA methylation, histone variants, small RNAs and transposable elements. We present examples of plant plasticity in the context of epigenetic regulation of developmental phases and transitions and map these onto the key stages of crop establishment, growth, floral initiation, pollination, seed set and maturation of harvestable product. In particular, we consider how feedback loops of environmental signals and plant nutrition affect plant ontogeny. Recent advances in understanding epigenetic processes enable us to take a fresh look at the crosstalk between regulatory systems that confer plasticity in the context of crop development. We propose that these insights into genotype × environment (G × E) interaction should underpin development of new crop management strategies, both in terms of information‐led agronomy and in recognizing the role of epigenetic variation in crop breeding.     

Iterative development and the scope for plasticity: contrasts among trait categories in an adaptive radiation

Phenotypic plasticity can influence evolutionary change in a lineage, ranging from facilitation of population persistence in a novel environment to directing the patterns of evolutionary change. As the specific nature of plasticity can impact evolutionary consequences, it is essential to consider how plasticity is manifested if we are to understand the contribution of plasticity to phenotypic evolution. Most morphological traits are developmentally plastic, irreversible, and generally considered to be costly, at least when the resultant phenotype is mis-matched to the environment. At the other extreme, behavioral phenotypes are typically activational (modifiable on very short time scales), and not immediately costly as they are produced by constitutive neural networks. Although patterns of morphological and behavioral plasticity are often compared, patterns of plasticity of life history phenotypes are rarely considered. Here we review patterns of plasticity in these trait categories within and among populations, comprising the adaptive radiation of the threespine stickleback fish Gasterosteus aculeatus. We immediately found it necessary to consider the possibility of iterated development, the concept that behavioral and life history trajectories can be repeatedly reset on activational (usually behavior) or developmental (usually life history) time frames, offering fine tuning of the response to environmental context. Morphology in stickleback is primarily reset only in that developmental trajectories can be altered as environments change over the course of development. As anticipated, the boundaries between the trait categories are not clear and are likely to be linked by shared, underlying physiological and genetic systems.     

Epigenetics underpins phenotypic plasticity of protandrous sex change in fish

Phenotypic plasticity is an important driver of species resilience. Often mediated by epigenetic changes, phenotypic plasticity enables individual genotypes to express variable phenotypes in response to environmental change. Barramundi (Lates calcarifer) are a protandrous (male‐first) sequential hermaphrodite that exhibits plasticity in length‐at‐sex change between geographic regions. This plasticity is likely to be mediated by changes in DNA methylation (DNAm), a well‐studied epigenetic modification. To investigate the relationships between length, sex, and DNAm in a sequential hermaphrodite, here, we compare DNAm in four conserved vertebrate sex‐determining genes in male and female barramundi of differing lengths from three geographic regions of northern Australia. Barramundi first mature as male and later sex change to female upon the attainment of a larger body size; however, a general pattern of increasing female‐specific DNAm markers with increasing length was not observed. Significant differences in DNAm between males and females of similar lengths suggest that female‐specific DNAm arises rapidly during sex change, rather than gradually with fish growth. The findings also reveal that region‐specific differences in length‐at‐sex change are accompanied by differences in DNAm and are consistent with variability in remotely sensed sea temperature and salinity. Together, these findings provide the first in situ evidence for epigenetically and environmentally mediated sex change in a protandrous hermaphrodite and offer significant insight into the molecular and ecological processes governing the marked and unique plasticity of sex in fish.