Skip to main content
NCBI home page
Wiley Open Access Collection logoLink to Wiley Open Access Collection
. 2025 Jan 12;106(1):e4503. doi: 10.1002/ecy.4503

Developmental plasticity does not improve performance during a species interaction: Implications for species turnover

Alexander A Mauro 1,2,✉, Kyndall R Zeller 3, Julián Torres‐Dowdall 4, Cameron K Ghalambor 1,2,3
PMCID: PMC11725713  PMID: 39800909

Abstract

Species interactions can contribute to species turnover when the outcomes of the interactions are context dependent (e.g., change along environmental gradients). Plasticity may change this dynamic by altering the environmental tolerances of the species interacting. Here, we explored how the competitive interaction between two euryhaline fish, Poecilia reticulata and Poecilia picta, is influenced by acute and developmental responses to salinity. In Trinidad, P. reticulata is confined to freshwater despite being tolerant of brackish water. P. reticulata may fail to occupy brackish water because of reduced tolerance to salinity or because P. picta competitively excludes them, and developing in brackish water could alter the dynamics of either scenario. To test this, we compared the salinity tolerances of both species in the absence of competition, reared P. reticulata individuals in freshwater or brackish water, and tested the consequences of developmental plasticity in experiments in which P. reticulata competed against conspecifics or P. picta during acute exposure to freshwater or brackish water. We found that (1) P. reticulata has a weaker salinity tolerance than P. picta; (2) P. reticulata that developed in freshwater perform best when competing against P. picta in freshwater but perform poorly when competing against P. picta in brackish water, suggesting the species interaction is context dependent; and (3) developing in brackish water did not benefit P. reticulata in brackish water. Our results suggest that P. reticulata's freshwater range limit is in part a product of a lower salinity tolerance leading to a decrease in competitive performance in brackish water. Adaptive plasticity has been suggested to be a crucial part of the colonization process, yet nonadaptive plastic responses as found here can limit range expansion and reinforce range limits.

Keywords: aggression, competition, developmental plasticity, fish, range limits, salinity

INTRODUCTION

A fundamental goal of ecology is to understand the mechanisms underlying the distribution of species. Early studies emphasized the importance of biotic interactions versus physiological tolerance to abiotic factors in shaping species distributions, patterns of community structure, and successional change, but often viewed these mechanisms as mutually exclusive (e.g., Clements, 1936; Gleason, 1926). These debates shaped the development of the “ecological niche” as a conceptual framework wherein tolerance to abiotic factors described the full range of environmental conditions that could be occupied, and biotic interactions could further limit these distributions. Specifically, ecological niche theory predicts that habitable areas within an organism's fundamental niche are often rendered uninhabitable by exclusion via interactions with other species (Chase & Leibold, 2003; Hutchinson, 1957; Thompson et al., 2021). Yet, distinguishing whether species are excluded from a given environment because of a lack of physiological tolerance versus species interactions can be difficult because both processes can interact with each other in a dynamic manner (e.g., Kraft et al., 2015).

One way species interactions and abiotic tolerance interact is when the outcome of species interactions changes depending on the environmental context (Chamberlain et al., 2014; Dunson & Travis, 1991; Mauro et al., 2022). Such “context‐dependent” species interactions arise either because species differ in tolerance to an environmental challenge and this indirectly impacts performance and/or because the environment directly alters the traits vital to performance during interactions (Mauro et al., 2022). However, identifying which mechanism(s) are at play can be difficult. For example, the competitive dominance of an invasive mosquitofish over a native cyprinodont is lost at higher salinities (Alcaraz et al., 2008). Yet, it is difficult to know if this is because of a direct effect of salinity on traits that determine competitive dominance via shared physiological control mechanisms (Mauro & Ghalambor, 2020), or, if reduced aggression is a secondary consequence of salinity stress. Understanding how the environment alters the outcome of species interactions can help explain why one species abruptly replaces another along an environmental gradient (Martin & Ghalambor, 2023; Means, 1975) and how the environment alters such interactions will depend on the mechanisms that impact interacting species (e.g., Connell, 1983; Dunson & Travis, 1991; Willi & Van Buskirk, 2019).

The concept of phenotypic plasticity provides a necessary conceptual framework to understand how tolerance to environmental stressor and the traits involved in species interactions (i.e., aggression, foraging, escape speed, etc.) change in response to specific environmental conditions (Agrawal, 2001). Broadly, phenotypic plasticity describes how the phenotype of a given genotype will predictably change in response to different environmental conditions (e.g., DeWitt & Scheiner, 2004) and is thus intimately related to niche breadth (Sexton et al., 2017). The developmental environment can result in phenotypic changes that persist into adulthood (i.e., developmental plasticity) and in turn impact tolerance and performance in response to environmental variation (Beaman et al., 2016; Gabriel, 2005; Piersma & Drent, 2003). Many physiological and behavioral traits are plastic and important in mediating species interactions by altering tolerance to an environmental stressor or by directly altering a trait critical to a species interaction (Gabriel, 2005; Mauro et al., 2022; Piersma & Drent, 2003; Richards et al., 2006). In particular, adaptive developmental plasticity in response to an environmental stressor can reduce the negative impacts of the stressor (Bateson et al., 2014; Donelson et al., 2012; Wilson et al., 2002), which could then alter context‐dependent species interactions. However, not all plastic responses are adaptive (Ghalambor et al., 2007), and the degree to which plasticity impacts niche breadth remains an open question (Sexton et al., 2017).

Here, we test whether developmental plasticity results in beneficial acclimation as it relates to a context‐dependent species interaction to better understand how developmental plasticity, the acute environment, and species interactions influence species turnover along environmental gradients. We explore this question in two species of euryhaline fish that segregate along a salinity gradient. Specifically, we investigate whether developing in brackish water improves the competitive performance of the Trinidadian guppy (Poecilia reticulata) when competing against the closely‐related swamp guppy (Poecilia picta) in brackish water.

Study system

On the island of Trinidad, P. reticulata is only found in freshwater (Torres‐Dowdall et al., 2013) despite existing in brackish water in other locations within its native and invasive range (Courtenay et al., 1974; Hulsman et al., 2008; Magurran, 2005) and surviving in seawater in the laboratory (Chiyokubo et al., 1998; Shikano et al., 2001; Shikano & Fujio, 1998). The abrupt range limit of P. reticulata occurs because they can behaviorally avoid salinity (Mauro et al., 2021) and do so in the wild by moving away from regular influxes of salinity from seasonal and tidal influences (Torres‐Dowdall et al., 2013). This abrupt range limit is repeated across all major rivers in Trinidad, making it a striking feature of the ecology of P. reticulata on Trinidad (Torres‐Dowdall et al., 2013). In contrast, the closely‐related species, P. picta, is primarily found in brackish water on Trinidad, but expands briefly into freshwater sections of rivers, where it is the only other Poecilid coexisting with P. reticulata (Magurran, 2005; Torres‐Dowdall et al., 2013). Hence, populations of P. reticulata at their natural range limit on Trinidad are faced with the combined eco‐physiological challenge of brackish water and the presence of a potential competitor.

The distributional pattern of P. reticulata has led to the working hypothesis that the combination of brackish water and competition with P. picta contributes to P. reticulata's freshwater range limit on Trinidad. Prior work found that P. reticulata transplanted to brackish water in nature had reduced survival only in the presence of P. picta, and laboratory experiments found P. reticulata are subordinate to P. picta in brackish water but not in freshwater (Mauro et al., 2021). However, experiments that link salinity tolerance with performance during acute exposure to salinity and competition have not been explored, nor has the potential role of developmental plasticity to alter these outcomes. Hence, we investigated this by first assessing each species' (P. reticulata/P. picta) tolerance to freshwater and brackish water in the absence of competition. We then assessed the change in body condition and behavior of P. reticulata in both salinities during intraspecific or interspecific competition and repeated those experiments on P. reticulata raised in either brackish water or freshwater. We predicted that if developing in brackish water results in an adaptive plastic response, then P. reticulata would exhibit improved performance in brackish water. Further, our experimental design allowed us to begin to unravel the mechanisms underlying how salinity alters interactions between P. reticulata and P. picta.

METHODS

Unless deviations are stated, the fish used in our experiments were P. reticulata and P. picta that were laboratory‐raised second‐generation (F2) descendants of fish taken from Trinidad in 2011 (growth rate experiment) or 2016/2017 (competition experiments). Wild fish were collected from a freshwater portion of the Caroni River where P. reticulata and P. picta are found together (see Appendix S1: Section S1 for detailed collection/experiment information). Wild fish were transported to Colorado State University and housed in 1.5‐L freshwater tanks on large recirculating systems (Ghalambor et al., 2015). They were kept on a 12:12 h light cycle under temperature conditions that mimicked Trinidad (25 ± 1°C) and in freshwater. Wild‐caught fish and F1 fish were fed amounts of food at our “medium level” (see next section) and F2 fish were fed in accordance with their experimental design.

Effect of salinity and food availability on growth rate in P. reticulata and P. picta

To test whether P. reticulata and P. picta exhibit baseline differences in their response to salinity stress, we tested how salinity and food availability impact growth rates independent of competitive interactions. The assumption was that if salinity stress imposed an energetic cost, it would be magnified under food limitation. Hence, we compared F2 full siblings raised under different combinations of salinity (freshwater vs. brackish water) and food levels (low, medium, and high) (Figure 1A). To generate F2s, we raised and then randomly mated the offspring of wild‐caught fish (F1s) in two salinity levels (0 and 20 psu), which meant that our experimental F2 fish were born at the salinity level in which they were tested. Within 24 h post‐parturition, F2 siblings were weighed, placed in individual tanks, and assigned to one of our three food levels (six total treatments: 2 salinities × 3 food levels). The medium food level consisted of daily food in the same quantity used by Reznick (1982) to achieve 85%–90% maximum growth rate. The high food level was twice as much food and the low food level was half as much food. The experiment included 28 P. reticulata families with 130 total P. reticulata (1–13 fish per family; average of 4.6 fish per family) and 26 P. picta families with 114 total P. picta (1–10 fish per family; average of 4.4 fish per family). To measure specific growth rate (SGR), we weighed fish at birth and then 28 days later and used the equation: SGR = ((LN (Mass_week4) − LN(Mass_birth))/28 days × 100) (Lugert et al., 2016). We investigated differences in SGR (response variable) using a linear mixed‐model ANOVA with species, food level, salinity, and all possible interactions as fixed factors and family as a random factor (intercept). Analyses were performed using the lme4 (Douglas et al., 2015) package in R version 4.2.2 (R Core Team, 2022). We ran post hoc means comparison tests between salinity treatments at each level of species and food level with a Tukey adjustment for multiple testing using the lsmeans package (Lenth, 2016) in R.

FIGURE 1.

FIGURE 1

Open in a new tab

(A) Both Poecilia reticulata (right six bars) and Poecilia picta (left six bars) had reduced growth in brackish water compared with freshwater, but the effect of salinity was more marked in P. reticulata and at lower food levels (Appendix S1: Table S1). At the high food level, salinity had no effect on growth in both species, but at the medium (Med) and low food levels, P. reticulata grew slower in brackish water than in freshwater, whereas there was only a trend for salinity to decrease growth in P. picta at the lowest food level (Appendix S1: Table S3). Means with 95% CIs are displayed and points represent individual data. (B) Brackish water‐developed P. reticulata (left four bars) lost more body condition than freshwater‐developed fish (right four bars) (Appendix S1: Table S4). During interspecific competition (“Inter”; “Intra” denotes intraspecific competition), freshwater‐developed P. reticulata gained more body condition in freshwater than in brackish water (Appendix S1: Table S5). Means with 95% CIs are displayed and points represent individual averages.

Effects of developmental and acute salinity, and competition on behavior and body condition

To investigate the effects of acute salinity, developmental salinity, and competitive environment on adult behavior and fitness, we measured change in body condition and aggressive behaviors. We used these metrics because body condition is a correlate of fitness that integrates access to food over time and aggressive behaviors provide a potential mechanism by which access to food is controlled. Following a 2 × 2 × 2 factorial design (see Appendix S1: Figure S1 for a representation of the design and ecological relevance of each treatment), we varied acute salinity (0 or 15 psu), competition type (P. reticulata vs. P. reticulata (intraspecific competition); or P. reticulata vs. P. picta (interspecific competition)), and developmental salinity (P. reticulata raised in 0 psu (freshwater developed); or 30 psu (brackish water developed)). Hence, we had eight total treatment groups and n = 4–14 individual P. reticulata per treatment (62 total individuals). We separated male siblings from 17 family lines across our eight treatments to account for the effect of genetic differences between families, but most family lines did not have eight male siblings, which led to an unbalanced design. As we were interested in how the population mean changes under different conditions while controlling for relatedness, we treated family as a random effect in our statistical models (Nussey et al., 2007). This approach allowed us to use more complex models, which increased our ability to analyze all individuals simultaneously and account for an unbalanced design.

The study fish in this experiment deviated from fish in the growth experiment in the following ways. The fish were all 12+ weeks old adult males that had been raised on the medium food level prior to the experiment. The freshwater‐developed F2 P. reticulata were in 0 psu from birth to maturation (12+ weeks), whereas brackish water‐developed F2s were born in 0 psu tanks and transferred to 15 psu tanks within 24 h of birth. They were further transferred to 30 psu tanks 1 week after birth and remained in 30 psu prior to the experiment. The P. picta used in brackish water competition experiments were F2 descendants of fish collected from Trinidad in 2016; however, they were taken from a brackish portion of the Caroni River that varied from 25 to 35 psu salinity. These fish were kept at a salinity of 30 psu but were otherwise housed and bred in the same fashion as other fish. The P. picta used in freshwater competition treatments were either wild caught, F1, or F2 individuals (due to a lack of F2 individuals). We did not observe behavioral differences between the generations, but did not have proper replication to formally test this potentially confounding variable. Importantly, prior studies on P. reticulata from Trinidad found no difference in behavior due to generation in the laboratory (Gorlick, 1976; Magurran & Seghers, 1991), and we assumed P. picta would similarly not display a generation effect.

Experiments began by taking baseline body condition measurements for each fish. Body condition was calculated using Peig and Green's (2009) “scaled mass index.” This index scales mass according to the length of each individual and the population mean, and it retains the original mass units (further details in Appendix S1: Section S2). Next, fish were transferred to 1.5‐L holding tanks (one fish per tank) at their rearing salinity for 48 h. To avoid any experimental group experiencing a salinity transfer of greater than ±15 psu at the beginning of the experiment, 30 psu developed P. reticulata competing in 0 psu were transferred to 15 psu holding tanks post body condition measurements and acclimated to 15 psu for 48 h. Following acclimation, all fish were transferred to 37‐L competition tanks (two fish per tank) at their experimental salinity (Appendix S1: Figure S1 diagram shows the salinity transfers for further clarity). The fish within each tank were size matched to the best of our ability because body size can alter the outcome of antagonistic interactions and any remaining differences in mass were further investigated.

After the transfer to experimental tanks, we measured behavior and body condition change over 3 weeks. Food was provided to each pair by placing 50% of the regular allotment of food (for two fish) on a single side of a centrally located dice‐sized block and aggressive behaviors between each pair of fish were recorded during 5‐min observations directly after feeding on Days 1, 2, 3, 4, 7, 14, and 21. Aggressive behaviors were combined into total counts for analysis and included nips, chases, monopolizing the food source, gonopodium swings, tail beatings, and fin flares (defined in Appendix S1: Section S3). Body condition was remeasured after behavioral observations on Days 7, 14, and 21.

Analyzing interspecific competition under different salinities

Differences in aggressive behavior provide insight into behavioral dominance in fish (Gilmour et al., 2005). Further, this metric controls for the fact that an individual's aggressive behavior is in part dependent on the behavior of their competitor. Hence, we analyzed the average difference in aggressive behaviors between P. reticulata/P. picta pairs (response variable) using a linear mixed‐model ANOVA with acute salinity, developmental salinity, and their interaction as fixed factors, and P. reticulata family as a random factor (intercept) using the package lme4 in R. We also ran a repeated measures model in which we incorporated the effect of time (observation day) on the difference in aggressive behaviors between P. reticulata/P. picta pairs; however, upon finding no effect of time, we opted to use the simpler “average” model instead. After finding no significant effect of developmental salinity nor its interaction with experimental salinity on our full model (see Results ) but seeing an apparent effect of acute salinity graphically, we split our data by developmental salinity to investigate the role of experimental salinity in both groups separately. We used a linear mixed‐model ANOVA with experimental salinity as a fixed factor and family as random factor (intercept) for the freshwater‐developed group and a linear model ANOVA with experimental salinity as a fixed factor for the brackish‐developed group (we were unable to incorporate family into this model due to lack of observations). We investigated the effect of size on behavior by testing for the effect of the difference in body mass between P. reticulata/P. picta pairs on the difference in aggressive behaviors between pairs. We did this via linear model ANOVAs (one for each developmental group) in which the starting difference in body mass and acute salinity were fixed factors and the difference in aggressive behaviors averaged across all observations was the response using lme4 in R.

Analyzing the effects of developmental and acute salinity, and competition on body condition

The average difference in body condition at the end of each week from the baseline measurement was used as the response variable in a mixed‐model ANOVA, with acute salinity, competition type, developmental salinity, and all possible interactions between those treatments as fixed factors and family and tank as random factors (intercepts). After finding that only developmental salinity and the acute salinity–competition interaction were significant, we ran post hoc tests to investigate what was driving the interaction. We conducted a post hoc least‐squared means comparison between the acute salinity treatments under each level of developmental salinity and competition type (with a Tukey adjustment) using lsmeans in R. Like with our analysis on aggression, we investigated a repeated measures model that incorporated the effect of time, but after finding no effect of time, we again opted for the simpler “averages” model. Lastly, we tested to see whether the effect of development could be an artifact of differing starting body conditions between development groups by running a linear mixed‐model ANOVA in which baseline body condition was the response, development group was a fixed factor, and family was a random factor (intercept).

Analyzing different competition types in P. reticulata

To compare how competition type (intra‐ vs. interspecific) differed in P. reticulata across acute salinity and developmental salinity, we tested how those factors affected total aggressive behavior counts. We ran an ANOVA on a generalized linear mixed model in which the average total aggression count was a response, acute salinity, competition, developmental salinity, and all possible two‐way interactions were fixed factors, and family was a random factor (intercept) using the glmer function from the lme4 package in R (distribution = Poisson, link = log).

RESULTS

Salinity affects growth more in P. reticulata than in P. picta

Both P. reticulata and P. picta had reduced growth in brackish water compared with freshwater (Salinity effect: F 1,231 = 30.83, p < 0.0001), but the effect of salinity was more marked in P. reticulata (Species effect: F 1,76 = 0.6532, p = 0.4224; Species × Salinity: F 1,232 = 10.47, p = 0.0014; Figure 1A) and at lower food levels (Food: F 2,218 = 236.7, p < 0.0001; Food level × Species: F 2,218 = 0.4965, p = 0.4965) (Figure 1A; Appendix S1: Table S1). Contrasts revealed that at the high food level, salinity had no effect on growth in both species (P. reticulata: T 221 = −1.784, p = 0.0757; P. picta: T 227 = 0.539, p = 0.5906), but at the medium and low food levels, P. reticulata grew slower in brackish water than in freshwater (Medium: T 214 = −4.396, p < 0.0001; Low: T 219 = −4.918, p < 0.0001), whereas there was only a trend for salinity to decrease growth in P. picta at the lowest food level (Low: T 232 = −0.670, p < 0.0631) (Figure 1A; Appendix S1: Tables S2 and S3).

Developmental salinity and acute salinity–competition interaction affect body condition

Across all treatments, brackish water‐developed P. reticulata lost more body condition than freshwater‐developed P. reticulata (F 1,33 = 11.30, p = 0.0019; Figure 1B; Appendix S1: Table S4). There was a significant acute salinity by competition interaction (F 1,34 = 5.770, p = 0.0219; Appendix S1: Table S4). Post hoc tests between acute salinities (fresh or brackish) within each level of development salinity (fresh or brackish) and competition (interspecific or intraspecific) found freshwater‐developed P. reticulata competing against P. picta gained more body condition in freshwater than in brackish water (T 42.7 = 2.319, p = 0.0253; Figure 1B; Appendix S1: Table S5). Three treatments had significant changes in body conditions (95% CIs do not overlap with 0.0, Figure 1B; Appendix S1: Table S6): brackish‐developed P. reticulata lost body condition when competing against P. picta in brackish water and when competing against conspecifics in freshwater, and freshwater‐developed P. reticulata gained body condition when competing against P. picta in freshwater. The effect of development on body condition was not likely due to differing baseline body conditions as there was no difference between development groups (F 1,51 = 0.3527, p = 0.5552; Appendix S1: Table S7).

Acute salinity affects the species interaction between P. reticulata and P. picta

Acute salinity affected the outcome of interspecific interactions between P. reticulata/P. picta pairs when P. reticulata developed in freshwater (F 1,9 = 16.74, p = 0.0029; Figure 2A; Appendix S1: Tables S8 and S9), but not when P. reticulata developed in brackish water (F 1,7 = 0.0673, p = 0.8028; Appendix S1: Tables S9 and S10). Freshwater‐developed P. reticulata exhibited significantly fewer aggressive behaviors than their P. picta partner in brackish water but exhibited a similar number of behaviors as their partner in freshwater (Figure 2A). There was no effect of difference in body mass between P. reticulata/P. picta pairs on the average difference in aggressive behaviors between those pairs for P. reticulata raised in freshwater (F 1,12 = 0.0605, p = 0.8099) or brackish water (F 1,6 = 0.9488, p = 0.8878, Appendix S1: Table S11).

FIGURE 2.

FIGURE 2

Open in a new tab

(A) Freshwater‐developed Poecilia reticulata were not dominant nor subordinate to Poecilia picta in freshwater but were subordinate to P. picta in brackish water as they displayed significantly fewer aggressive behaviors. Brackish water‐developed P. reticulata were not dominant nor subordinate to P. picta in both acute salinities (Appendix S1: Table S9). Means with 95% CIs are displayed and points represent individual averages. (B) P. reticulata were more aggressive in intraspecific treatments (right four bars) than in interspecific treatments (left four bars), averaged across both acute and developmental salinities (freshwater and brackish water) (Appendix S1: Table S12). Means with 95% CIs are displayed and points represent individual averages.

Intraspecific interactions were greater than interspecific ones in P. reticulata

P. reticulata exhibited more aggressive behaviors during intraspecific interactions than during interspecific interactions with P. picta regardless of acute salinity or developmental salinity (χ2 = 4.596, df = 1, p = 0.0320; Figure 2B; Appendix S1: Table S12) (see Appendix S1: Figure S2, Table S13 for corresponding P. picta results).

DISCUSSION

In Trinidad, P. reticulata is restricted to freshwater and actively avoids brackish water, whereas P. picta is largely found in brackish water but coexists with P. reticulata in a narrow band of freshwater where freshwater transitions to brackish water (Torres‐Dowdall et al., 2013). Previous work (Mauro et al., 2021; Torres‐Dowdall et al., 2013) led us to hypothesize that P. reticulata's abrupt range limit is due to the combined effects of brackish water and competition with P. picta. We found support for this hypothesis by showing that (1) P. reticulata are less tolerant of salinity stress than P. picta, particularly when food is limited (Figure 1A); (2) P. reticulata is subordinate to P. picta in brackish water but not freshwater (Figure 2A); and (3) this change in dominance is associated with a change in body condition in P. reticulata (Figure 1B). We found developing in brackish water did not improve P. reticulata performance in brackish water but developing in freshwater was beneficial for P. reticulata in freshwater (Figures 1B and 2A). Collectively, these results argue that acclimation to brackish water (i.e., developmental plasticity) is unable to overcome the combined stress of elevated salinity and competition with P. picta.

Differing baseline physiological tolerances and the outcome of competitive interactions

In the absence of competition, P. reticulata and P. picta differ in their tolerance to salinity, but this is dependent on food availability. When given excess food, both species achieved their highest growth rates regardless of the salinity (Figure 1A), consistent with the view that both species are euryhaline. However, when food levels were reduced and growth rate declined, the effect of salinity on growth was greater in P. reticulata than in P. picta (Figure 1A). Osmoregulation can take up large portions of fish energy budgets at the cost of growth (e.g., Bœuf & Payan, 2001), hence these results suggest that both P. reticulata and P. picta at the range‐edge prefer freshwater, but P. picta is more tolerant of brackish water.

Given that reduced food increases salinity stress, the competitive interaction over food between P. reticulata and P. picta across salinity may be important in this system. This is reflected in our competition experiments. When freshwater‐developed P. reticulata compete against P. picta in freshwater, they gain body condition (Figure 1B) while exhibiting a similar number of aggressive behaviors as P. picta (Figure 2A), suggesting P. reticulata may have a competitive advantage over P. picta in freshwater (Mauro et al., 2021). However, when freshwater‐developed P. reticulata compete with P. picta in brackish water, they can only maintain body condition (Figure 1B) and exhibit fewer aggressive behaviors than P. picta and could thus be considered subordinate (Gilmour et al., 2005) (Figure 2A). Hence, P. reticulata's avoidance of brackish water (Mauro et al., 2021) may be to avoid the combined stress of salinity and interspecific competition. Consistent with prior results (Mauro et al., 2021), these results suggest that P. reticulata lose their relative advantage over P. picta in brackish water, and thus the colonization of brackish water would be challenging for freshwater‐developed P. reticulata.

We hypothesize that differing baseline tolerances to salinity underly the context dependency of the P. reticulata–P. picta interaction. Specifically, we hypothesize that the stress of brackish water exposure indirectly impacts performance to a greater degree in P. reticulata than in P. picta because of the increased energetic cost of coping with salinity stress in P. reticulata compared with P. picta. This perspective is consistent with the idea that when tolerance to an environmental stressor is energy‐dependent, it can influence distribution limits because elevated maintenance costs from environmental stress reduce energy available for other ecologically important tasks (growth, reproduction, competition) needed to maintain a population (Brown et al., 2004; Schulte, 2015; Sokolova, 2013). This is especially pertinent in our system because the trade‐off associated with osmoregulation and growth (e.g., Bœuf & Payan, 2001) should be elevated if access to food is restricted via competitive interactions (see Figure 2A).

Elevated energetic costs also provide an explanation for a potential disconnect between our behavior and body condition results. We predicted that gaining body condition during a competitive interaction requires behavioral dominance, and conversely, if a species is subordinate, then they would lose body condition. Our results do not quite match these predictions (Figures 1B and 2A). However, if P. reticulata's lower growth rate in brackish water (Figure 1A) reflects greater basal energy expenditure in brackish water, then maintaining body condition in brackish water (as we observe) would come at the cost of energy spent on other functions, like aggression during competition (as we observe). In the short term or in benign environments, sacrificing competitive ability to maintain body condition can be an optimal strategy for subordinate fish (Clarke, 1992; Metcalfe, 1986). But, in the long term or in stressful environments, this strategy may fail as fish fail to satisfy minimum energy demands.

Asymmetric competition and species turnover along an environmental gradient

The distribution pattern of P. reticulata and P. picta in nature, their differences in baseline salinity tolerances, and their competitive interaction are consistent with the conditions models predict for “stable range limits” among competing species distributed along an environmental gradient (e.g., Adler et al., 2018; Barabás et al., 2016; Case & Taper, 2000; Price & Kirkpatrick, 2009). In particular, our results showing that P. reticulata's relative fitness advantage over P. picta is salinity dependent (Figures 1B and 2A) and that intraspecific competition in P. reticulata is greater than interspecific competition regardless of environment (Figure 2B), are common characteristics of coexisting species (Adler et al., 2018, Barabás et al., 2016). Our results are also consistent with the common pattern in which species turnover along an environmental gradient because one species has a broad environmental tolerance (P. picta), but is largely competitively excluded from its preferred environment (freshwater) by a dominant species with a more narrow environmental tolerance (P. reticulata) (Martin & Ghalambor, 2023).

Still, systematically testing the mechanisms underlying how an environmental gradient (i.e., salinity) and competition shape species turnover and range limits is challenging, and ultimately more experiments are needed in our system. First, it would be necessary to experimentally link physiological stress (metabolic rate, energy balance, etc.) to salinity and population vital rates in our study species (i.e., Sokolova, 2013). Second, it would be necessary to measure if variation in stress responses explains variation in competitive exclusion ability in both P. picta and P. reticulata across salinity (Mauro et al., 2022). Finally, reciprocal removal experiments could be used to test how these mechanisms play out in nature (Martin & Ghalambor, 2023). While such tests remain to be conducted, this study provides insight into how physiological differences between P. reticulata and P. picta impact the outcome of their competitive interaction across salinities and how that relates to P. reticulata's range in nature.

Nonadaptive developmental plasticity in the context of distribution limits

Adaptive phenotypic plasticity is argued to enhance niche breadth through the environmentally induced expression of phenotypes adapted to a wider array of environments (Richards et al., 2005; Sexton et al., 2017; Stearns, 1989; Sultan, 2001). Yet, whether plasticity is adaptive or nonadaptive in response to environmental change (e.g., Ghalambor et al., 2007; Wilson et al., 2002) and its relative importance in colonization/range expansion (Bozinovic et al., 2011; Lande, 2015) are long‐standing questions in ecology. We found developmental plasticity was only adaptive when P. reticulata developed in its “home” freshwater environment and largely nonadaptive when they developed in the “away” brackish water environment. Freshwater‐developed P. reticulata gained body condition when competing against P. picta in freshwater and maintained condition in all other treatments (Figure 1B), suggesting that developing in freshwater is adaptive as it allows P. reticulata to maintain body condition even when exposed to the acute effects of brackish water regardless of the type of interaction (intra‐ vs. interspecific). In contrast, development in brackish water resulted in a trend for a loss in condition across all treatments (Figure 1B). Thus, not only was there no benefit of developing in brackish water, but the general pattern was for a reduction in body condition regardless of acute salinity (Figure 1B). Lastly, developing in brackish water does not appear to benefit P. reticulata in terms of its behavior toward P. picta. Because the 95% CIs of the difference in aggressive behaviors overlap zero in both salinities for brackish water‐developed P. reticulata (Figure 2A), it suggests neither species is dominant; however, we posit this is due to low power in our analysis (low sample size) and argue that brackish water‐developed P. reticulata are likely subordinate across salinities as the average values for both treatments are far below zero.

Plasticity's role in moderating species coexistence and community dynamics is a rapidly growing area of research in which trait‐based approaches are being used both empirically and theoretically (Berg & Ellers, 2010; Fey et al., 2021; Gómez et al., 2023; Miner et al., 2005). However, much of this work has focused only on how acute adaptive plasticity is effective in expanding the realized niche of populations and the corresponding ecological consequences (Sexton et al., 2017). Our results suggest developmental plasticity to salinity can be both adaptive (freshwater) and nonadaptive (brackish water) (see Lee & Petersen, 2003 for a similar result in a copepod). Theoretical work predicts this pattern of plasticity would constrain P. reticulata's ability to colonize brackish water in the presence of a competitor species while also constraining the realized niche of the competitor species in freshwater (Lande, 2015; Peacor et al., 2006).

CONCLUSION

This study is consistent with a growing literature that shows plasticity to stressful environments can be nonadaptive (e.g., Ghalambor et al., 2007; Luhring et al., 2019; Ramniwas et al., 2020) and underlies the importance of studying plasticity when investigating range limits and species interactions (Berg & Ellers, 2010; Miner et al., 2005). Consistent with the distributions of P. reticulata in Trinidad (Torres‐Dowdall et al., 2013), our results suggest expansion into brackish water would be challenging for P. reticulata. Like with prior research (Mauro et al., 2021), we found support for the hypothesis that the combination of brackish water and competition with P. picta contributes to P. reticulata's current freshwater range limit. Further, it appears that P. reticulata individuals would have difficulty establishing a population if they disperse into brackish water regardless of their developmental salinity because juvenile fish developing in brackish water grew poorly (Figure 1A) and then performed as poorly or worse as freshwater‐developed adults during competition experiments in brackish water (Figure 1B). However, we caution an overly broad interpretation of our results. Only one population of P. reticulata and P. picta from only one river were used in this study, and other populations could differ in their responses. Yet, we would not anticipate dramatically different results among populations based on the consistent distribution of P. reticulata and P. picta across Trinidad, the potential for high population connectivity between P. picta populations within and between rivers (Torres‐Dowdall et al., 2013; personal observations by authors), and the conserved physiological basis of salinity tolerance and aggression in fish (e.g., Evans et al., 2013; Gilmour et al., 2005; Mauro & Ghalambor, 2020). Nevertheless, documenting interpopulation variation in plasticity will be crucial when validating theory with empirical results and when making predictions of species‐level responses to environmental change (Forsman, 2015; Nussey et al., 2007). Lastly, a lower developmental salinity treatment (<30 psu) could lead to different results. Salinity levels in the swamps and rivers of Trinidad can vary dramatically (Torres‐Dowdall et al., 2013) and a lower salinity (<15 psu) could better reflect the salinity that P. reticulata colonizers might experience. Here and in general, research aimed at finer scale documentation of performance along environmental gradients will benefit our ability to relate laboratory results to predictions of range limits in nature (e.g., Troia & Gido, 2015).

AUTHOR CONTRIBUTIONS

Alexander A. Mauro, Julián Torres‐Dowdall, and Cameron K. Ghalambor designed experiments. Alexander A. Mauro, Julián Torres‐Dowdall, and Kyndall R. Zeller collected fish and bred fish. Alexander A. Mauro, Julián Torres‐Dowdall, and Kyndall R. Zeller collected data. Alexander A. Mauro performed analyses. Alexander A. Mauro and Kyndall R. Zeller wrote the manuscript. All authors contributed to revisions.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

Supporting information

Appendix S1.

ECY-106-e4503-s001.pdf (582.8KB, pdf)

ACKNOWLEDGMENTS

This work was supported by the National Science Foundation (NSF) grant (IOS‐1457383) to Cameron K. Ghalambor and a fellowship awarded to Alexander A. Mauro that is included in NSF grant (DGE‐1450032). All procedures were conducted under the approval of Colorado State University Animal Care and Use Committee (protocol no. 17‐7197A), and The Fisheries Division of the Ministry of Food Production, Land and Marine Affairs of Trinidad and Tobago. We thank Courtney Painter, Stazi Snelling, Jovan Vincent, Amber McCardle, Yared Belay, Craig Marshall, Richard Evans, and Porsche Robison for helping collect/care for guppies before and during experiments. We thank Lisa Angeloni and Dale Broder for assisting in designing experiments.

Mauro, Alexander A. , Zeller Kyndall R., Torres‐Dowdall Julián, and Ghalambor Cameron K.. 2025. “Developmental Plasticity Does Not Improve Performance during a Species Interaction: Implications for Species Turnover.” Ecology 106(1): e4503. 10.1002/ecy.4503

Handling Editor: Daniel E. Schindler

Alexander A. Mauro and Kyndall R. Zeller are co‐first authors.

DATA AVAILABILITY STATEMENT

Data (Mauro et al., 2024) are available in Dryad at https://doi.org/10.5061/dryad.vmcvdnd23.

REFERENCES

  1. Adler, P. B. , Smull D., Beard K. H., Choi R. T., and Meiners J. M.. 2018. “Competition and Coexistence in Plant Communities: Intraspecific Competition Is Stronger than Interspecific Competition.” Ecology Letters 21: 1319–1329. [DOI] [PubMed] [Google Scholar]
  2. Agrawal, A. A. 2001. “Phenotypic Plasticity in the Interactions and Evolution of Species.” Science 294: 321–326. [DOI] [PubMed] [Google Scholar]
  3. Alcaraz, C. , Bisazza A., and García‐Berthou E.. 2008. “Salinity Mediates the Competitive Interactions between Invasive Mosquitofish and an Endangered Fish.” Oecologia 155: 205–213. [DOI] [PubMed] [Google Scholar]
  4. Barabás, G. , Michalska‐Smith M. J., and Allesina S.. 2016. “The Effect of Intra‐ and Interspecific Competition on Coexistence in Multispecies Communities.” American Naturalist 188: E1–E12. [DOI] [PubMed] [Google Scholar]
  5. Bateson, P. , Gluckman P., and Hanson M.. 2014. “The Biology of Developmental Plasticity and the Predictive Adaptive Response Hypothesis.” Journal of Physiology 592: 2357–2368. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Beaman, J. E. , White C. R., and Seebacher F.. 2016. “Evolution of Plasticity: Mechanistic Link between Development and Reversible Acclimation.” Trends in Ecology & Evolution 31: 237–249. [DOI] [PubMed] [Google Scholar]
  7. Berg, M. P. , and Ellers J.. 2010. “Trait Plasticity in Species Interactions: A Driving Force of Community Dynamics.” Evolutionary Ecology 24: 617–629. [Google Scholar]
  8. Bœuf, G. , and Payan P.. 2001. “How Should Salinity Influence Fish Growth?” Comparative Biochemistry and Physiology Part C 130: 411–423. [DOI] [PubMed] [Google Scholar]
  9. Bozinovic, F. , Calosi P., and Spicer J. I.. 2011. “Physiological Correlates of Geographic Range in Animals.” Annual Review of Ecology, Evolution, and Systematics 42: 155–179. [Google Scholar]
  10. Brown, J. H. , Gillooly J. F., Allen A. P., Savage V. M., and West G. B.. 2004. “Toward a Metabolic Theory of Ecology.” Ecology 85: 1771–1789. [Google Scholar]
  11. Case, T. J. , and Taper M. L.. 2000. “Competition, Environmental Gradients, Gene Flow and the Coevolution of Species Borders.” The American Naturalist 155: 583–605. [DOI] [PubMed] [Google Scholar]
  12. Chamberlain, S. A. , Bronstein J. L., and Rudgers J. A.. 2014. “How Context Dependent Are Species Interactions?” Ecology Letters 17: 881–890. [DOI] [PubMed] [Google Scholar]
  13. Chase, J. M. , and Leibold M. A.. 2003. Ecological Niches: Linking Classical and Contemporary Approaches. Chicago: University of Chicago Press. [Google Scholar]
  14. Chiyokubo, T. , Shikano T., Nakajima M., and Fujio Y.. 1998. “Genetic Features of Salinity Tolerance in Wild and Domestic Guppies (Poecilia reticulata).” Aquaculture 167: 339–348. [Google Scholar]
  15. Clarke, R. D. 1992. “Coral Reefs Growth and Fecundity of Two Competing Coral Reef Fishes.” Coral Reefs 11: 199–205. [Google Scholar]
  16. Clements, F. E. 1936. “Nature and Structure of the Climax.” Journal of Ecology 24: 252–284. [Google Scholar]
  17. Connell, J. H. 1983. “On the Prevalence and Relative Importance of Interspecific Competition: Evidence from Field Experiments.” The American Naturalist 122: 661–696. [Google Scholar]
  18. Courtenay, W. R. , Sahlman H. F., Miley W. W., and Herrema D. J.. 1974. “Exotic Fishes in Fresh and Brackish Waters of Florida.” Biological Conservation 6: 292–302. [Google Scholar]
  19. DeWitt, T. J. , and Scheiner S. M., eds. 2004. “Phenotypic Variation from Single Genotypes: A Primer.” In Phenotypic Plasticity: Functional and Conceptual Approaches 1–9. New York, NY: Oxford University Press. [Google Scholar]
  20. Donelson, J. M. , Munday P. L., McCormick M. I., and Pitcher C. R.. 2012. “Rapid Transgenerational Acclimation of a Tropical Reef Fish to Climate Change.” Nature Climate Change 2: 30–32. [Google Scholar]
  21. Douglas, B. , Maechler M., Bolker B., and Walker S.. 2015. “Fitting Linear Mixed‐Effects Models Using lme4.” Journal of Statistical Software 67: 1–48. [Google Scholar]
  22. Dunson, W. A. , and Travis J.. 1991. “The Role of Abiotic Factors in Community Organization.” American Naturalist 138: 1067–1091. [Google Scholar]
  23. Evans, D. , Claiborne J., and Currie S.. 2013. The Physiology of Fishes. CRC Marine Biology Series. Boca Raton, FL: Taylor & Francis. [Google Scholar]
  24. Fey, S. B. , Kremer C. T., Layden T. J., and Vasseur D. A.. 2021. “Resolving the Consequences of Gradual Phenotypic Plasticity for Populations in Variable Environments.” Ecological Monographs 91: 1–14.35309738 [Google Scholar]
  25. Forsman, A. 2015. “Rethinking Phenotypic Plasticity and Its Consequences for Individuals, Populations and Species.” Heredity 115: 276–284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gabriel, W. 2005. “How Stress Selects for Reversible Phenotypic Plasticity.” Journal of Evolutionary Biology 18: 873–883. [DOI] [PubMed] [Google Scholar]
  27. Ghalambor, C. K. , McKay J. K., Carroll S. P., and Reznick D. N.. 2007. “Adaptive Versus Non‐Adaptive Phenotypic Plasticity and the Potential for Contemporary Adaptation in New Environments.” Functional Ecology 21: 394–407. [Google Scholar]
  28. Ghalambor, C. K. , Hoke K. L., Ruell E. W., Fischer E. K., Reznick D. N., and Hughes K. A.. 2015. “Non‐Adaptive Plasticity Potentiates Rapid Adaptive Evolution of Gene Expression in Nature.” Nature 525: 372–375. [DOI] [PubMed] [Google Scholar]
  29. Gilmour, K. M. , DiBattista J. D., and Thomas J. B.. 2005. “Physiological Causes and Consequences of Social Status in Salmonid Fish.” Integrative and Comparative Biology 45: 263–273. [DOI] [PubMed] [Google Scholar]
  30. Gleason, H. 1926. “The Individualistic Concept of the Plant Association.” Bulletin of the Torrey Botanical Club 53: 7–26. [Google Scholar]
  31. Gorlick, D. L. 1976. “Dominance Hierarchies and Factors Influencing Dominance in the Guppy Poecilia reticulata (Peters).” Animal Behaviour 24: 336–346. [Google Scholar]
  32. Gómez, J. M. , González‐Megías A., Armas C., Narbona E., Navarro L., and Perfectti F.. 2023. “The Role of Phenotypic Plasticity in Shaping Ecological Networks.” Ecology Letters 26: S47–S61. [DOI] [PubMed] [Google Scholar]
  33. Hulsman, H. , Vonk R., Aliabadian M., Debrot A. O., and Nijman V.. 2008. “Effect of Introduced Species and Habitat Alteration on the Occurrence and Distribution of Euryhaline Fishes in Fresh‐ and Brackish‐Water Habitats on Aruba, Bonaire and Curaçao (South Caribbean).” Contributions to Zoology 77(1): 45–51. [Google Scholar]
  34. Hutchinson, E. G. 1957. “Population studies‐animal ecology and demography‐concluding remarks.” Cold Spring Harbor symposia on quantitative biology. Vol. 22. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, Publications Department. [Google Scholar]
  35. Kraft, N. J. B. , Adler P. B., Godoy O., James E. C., Fuller S., and Levine J. M.. 2015. “Community Assembly, Coexistence and the Environmental Filtering Metaphor.” Functional Ecology 29: 592–599. [Google Scholar]
  36. Lande, R. 2015. “Evolution of Phenotypic Plasticity in Colonizing Species.” Molecular Ecology 24: 2038–2045. [DOI] [PubMed] [Google Scholar]
  37. Lee, C. E. , and Petersen C. H.. 2003. “Effects of Developmental Acclimation on Adult Salinity Tolerance in the Freshwater‐Invading Copepod Eurytemora Affinis.” Physiological and Biochemical Zoology 76: 296–301. [DOI] [PubMed] [Google Scholar]
  38. Lenth, R. 2016. “Least‐Squares Means: The R Package Lsmeans.” Journal of Statistical Software 69: 1–33. [Google Scholar]
  39. Lugert, V. , G. Thaller, J. Tetens, C. Schulz, and J. Krieter. 2016. “A Review on Fish Growth Calculation: Multiple Functions in Fish Production and Their Specific Application.” Reviews in Aquaculture 8: 30–42. [Google Scholar]
  40. Luhring, T. M. , Vavra J. M., Cressler C. E., and DeLong J. P.. 2019. “Phenotypically Plastic Responses to Predation Risk Are Temperature Dependent.” Oecologia 191: 709–719. [DOI] [PubMed] [Google Scholar]
  41. Magurran, A. E. 2005. Evolutionary Ecology: The Trinidadian Guppy. New York, NY: Oxford University Press Inc. [Google Scholar]
  42. Magurran, A. E. , and Seghers B.. 1991. “Variation in Schooling and Aggression Amongst Guppy (Poecilia reticulata) Populations in Trinidad.” Behaviour 118: 214–234. [Google Scholar]
  43. Martin, P. R. , and Ghalambor C. K.. 2023. “A Case for the “Competitive Exclusion–Tolerance Rule” as a General Cause of Species Turnover along Environmental Gradients.” The American Naturalist 202: 1–17. [DOI] [PubMed] [Google Scholar]
  44. Mauro, A. A. , Shah A. A., Martin P. R., and Ghalambor C. K.. 2022. “An Integrative Perspective on the Mechanistic Basis of Context‐Dependent Species Interactions.” Integrative and Comparative Biology 0: 1–15. [DOI] [PubMed] [Google Scholar]
  45. Mauro, A. A. , and Ghalambor C. K.. 2020. “Trade‐Offs, Pleiotropy, and Shared Molecular Pathways: A Unified View of Constraints on Adaptation.” Integrative and Comparative Biology 60: 332–347. [DOI] [PubMed] [Google Scholar]
  46. Mauro, A. A. , Torres‐Dowdall J., Marshall C., and Ghalambor C. K.. 2021. “A Genetically Based Ecological Trade‐Off Contributes to Setting a Geographic Range Limit.” Ecology Letters 24: 2739–2749. [DOI] [PubMed] [Google Scholar]
  47. Mauro, A. A. , Zeller K., Torres‐Dowdall J., and Ghalambor C.. 2024. “Developmental Plasticity Does Not Improve Performance during a Species Interaction: Implications for Species Turnover.” Dataset. Dryad. 10.5061/dryad.vmcvdnd23. [DOI] [PMC free article] [PubMed]
  48. Means, D. B. 1975. “Competitive Exclusion along a Habitat Gradient between Two Species of Salamanders (Desmognathus) in Western Florida.” Journal of Biogeography 2: 253. [Google Scholar]
  49. Metcalfe, N. B. 1986. “Intraspecific Variation in Competitive Ability and Food Intake in Salmonids: Consequences for Energy Budgets and Growth Rates.” Journal of Fish Biology 28: 525–531. [Google Scholar]
  50. Miner, B. G. , Sultan S. E., Morgan S. G., Padilla D. K., and Relyea R. A.. 2005. “Ecological Consequences of Phenotypic Plasticity.” Trends in Ecology & Evolution 20: 685–692. [DOI] [PubMed] [Google Scholar]
  51. Nussey, D. H. , Wilson A. J., and Brommer J. E.. 2007. “The Evolutionary Ecology of Individual Phenotypic Plasticity in Wild Populations.” Journal of Evolutionary Biology 20: 831–844. [DOI] [PubMed] [Google Scholar]
  52. Peacor, S. D. , Allesina S., Riolo R. L., and Pascual M.. 2006. “Phenotypic Plasticity Opposes Species Invasions by Altering Fitness Surface.” PLoS Biology 4: 2112–2120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Peig, J. , and Green A. J.. 2009. “New Perspectives for Estimating Body Condition from Mass/Length Data: The Scaled Mass Index as an Alternative Method.” Oikos 118: 1883–1891. [Google Scholar]
  54. Piersma, T. , and Drent J.. 2003. “Phenotypic Flexibility and the Evolution of Organismal Design.” Trends in Ecology & Evolution 18: 228–233. [Google Scholar]
  55. Price, T. D. , and Kirkpatrick M.. 2009. “Evolutionarily Stable Range Limits Set by Interspecific Competition.” Proceedings of the Royal Society B: Biological Sciences 276: 1429–1434. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. R Core Team . 2022. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. [Google Scholar]
  57. Ramniwas, S. , Kumar G., and Singh D.. 2020. “Rejection of the Beneficial Acclimation Hypothesis (BAH) for Short Term Heat Acclimation in Drosophila nepalensis .” Genetica 148: 173–182. [DOI] [PubMed] [Google Scholar]
  58. Reznick, D. 1982. “Genetic Determination of Offspring Size in the Guppy (Poecilia reticulata).” The American Naturalist 120: 181–188. [Google Scholar]
  59. Richards, C. L. , Bossdorf O., Muth N. Z., Gurevitch J., and Pigliucci M.. 2006. “Jack of all Trades, Master of Some? On the Role of Phenotypic Plasticity in Plant Invasions.” Ecology Letters 9: 981–993. [DOI] [PubMed] [Google Scholar]
  60. Richards, C. L. , Pennings S. C., and Donovan L. A.. 2005. “Habitat Range and Phenotypic Variation in Salt Marsh Plants.” Plant Ecology 176: 263–273. [Google Scholar]
  61. Schulte, P. M. 2015. “The Effects of Temperature on Aerobic Metabolism: Towards a Mechanistic Understanding of the Responses of Ectotherms to a Changing Environment.” Journal of Experimental Biology 218: 1856–1866. [DOI] [PubMed] [Google Scholar]
  62. Sexton, J. P. , Montiel J., Shay J. E., Stephens M. R., and Slatyer R. A.. 2017. “Evolution of Ecological Niche Breadth.” Annual Review of Ecology, Evolution, and Systematics 48: 183–206. [Google Scholar]
  63. Shikano, T. , and Fujio Y.. 1998. “Relationships of Salinity Tolerance to Immunolocalization of Na+,K(+)‐ATPase in the Gill Epithelium during Seawater and Freshwater Adaptation of the Guppy, Poecilia reticulata .” Zoological Science 15: 35–41. [DOI] [PubMed] [Google Scholar]
  64. Shikano, T. , Chiyokubo T., and Taniguchi N.. 2001. “Effect of Inbreeding on Salinity Tolerance in the Guppy (Poecilia reticulata).” Aquaculture 202: 45–55. [Google Scholar]
  65. Sokolova, I. M. 2013. “Energy‐Limited Tolerance to Stress as a Conceptual Framework to Integrate the Effects of Multiple Stressors.” Integrative and Comparative Biology 53: 597–608. [DOI] [PubMed] [Google Scholar]
  66. Stearns, S. C. 1989. “Trade‐Offs in Life‐History Evolution.” Functional Ecology 3: 259. [Google Scholar]
  67. Sultan, S. E. 2001. “Phenotypic Plasticity for Fitness Components in Polygonum Species of Contrasting Ecological Breadth.” Ecology 82: 328–343. [Google Scholar]
  68. Thompson, P. , Hürlemann S., and Altermatt F.. 2021. “Species Interactions Limit the Predictability of Community Responses to Environmental Change.” American Naturalist 198: 694–705. [DOI] [PubMed] [Google Scholar]
  69. Torres‐Dowdall, J. , Dargent F., Handelsman C. A., Ramnarine I. W., and Ghalambor C. K.. 2013. “Ecological Correlates of the Distribution Limits of Two Poeciliid Species along a Salinity Gradient.” Biological Journal of the Linnean Society 108: 790–805. [Google Scholar]
  70. Troia, M. J. , and Gido K. B.. 2015. “Functional Strategies Drive Community Assembly of Stream Fishes along Environmental Gradients and across Spatial Scales.” Oecologia 177: 545–559. [DOI] [PubMed] [Google Scholar]
  71. Willi, Y. , and Van Buskirk J.. 2019. “A Practical Guide to the Study of Distribution Limits.” The American Naturalist 193: 773–785. [DOI] [PubMed] [Google Scholar]
  72. Wilson, R. S. , Franklin C. E., and Franklin C. E.. 2002. “Testing the Beneficial Acclimation Hypothesis.” Trends in Ecology & Evolution 17: 66–70. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Appendix S1.

ECY-106-e4503-s001.pdf (582.8KB, pdf)

Data Availability Statement

Data (Mauro et al., 2024) are available in Dryad at https://doi.org/10.5061/dryad.vmcvdnd23.

Articles from Ecology are provided here courtesy of Wiley

RESOURCES