Plastic juvenile growth rates and offspring size: A response to anthropogenic shifts in prey size among populations

doi:10.21203/rs.3.rs-3208290/v1

Download PDF

Research Article

Plastic juvenile growth rates and offspring size: A response to anthropogenic shifts in prey size among populations

https://doi.org/10.21203/rs.3.rs-3208290/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 20 Sep, 2024

Read the published version in Oecologia →

You are reading this latest preprint version

Variation in prey characteristics among populations is frequently associated with similar variation in predator body sizes. Increasingly, human-mediated alterations in prey landscapes impose unique ecological pressures on predators that may lead to rapid shifts in predator body size. Here, we ask whether adult body size differences among populations are the product of genetic adaptation or phenotypic plasticity of juvenile growth in response to human-altered prey size differences. Using a common-garden design, we measured growth rates of neonate diamond-backed watersnakes (Nerodia rhombifer) from fish farms populations that vary substantially in prey size distributions. We also investigated the influence of initial offspring size differences on growth rate. We found that juvenile growth rates were faster for snakes from populations with access to larger average prey sizes. Our data suggest that these differences are the product of phenotypic plasticity, mediated through differences in initial size and prey consumption. Population-level differences in growth rate were not detected when initial size and prey mass consumed were included in the model. We propose that larger offspring sizes may favor increased growth rates, mediated through a larger energy processing capacity relative to smaller individuals. This experiment provides evidence supporting the growing body of literature that adaptive plasticity may be a significant driver of rapid phenotypic divergence among populations across a landscape. This mechanism may explain the stability and colonization of populations in the face of rapid, human-mediated, landscape changes.

Growth rate

phenotypic plasticity

body size

gape-limited predator

watersnake

Adult body size is an important correlate of many important life-history traits that dictate fitness (Blanckenhorn 2000, LaBarbera 1989, Roff 1992, Stearns 1992, Tibblin et al. 2015). Substantial research effort has focused on understanding the selective factors favoring population-level differences in adult body sizes. Population-level differences in adult body size have been correlated with thermal clines (Sears and Angilletta 2004, de Jong and Imasheva 2001, Lindmark et al 2018), latitude (Ashton 2004, Stillwell 2015), predation (Brooks and Dodson 1965, Blumenshine et al. 2000), competition (Aarssen 2015, Smith and Brown 1986) and resource availability (Jessop et al. 2006, Palkovacs 2003). Gape-limited predators, like snakes and fish, make excellent models to examine causes of body size variation. In this group of predators, studies have established strong correlations between population-level body size variation and the prey characteristics (i.e. prey size or prey density) to which the population has access (Aubret 2012, Aubret and Shine 2007, Boback 2003, Keogh et al 2005, Forsman 1991, Jessop et al. 2006, King et al 2006, Madsen and Shine 1993, Madsen and Shine 2000, Sun et al. 2002).

Prey characteristics provide interesting systems for examining variation of adult body sizes because they frequently vary substantially across the ecological landscape and from population to population. While many natural factors may cause prey characteristics to vary, anthropogenic causes are particularly important in light of the increasing interactions between wildlife and humans. The types of anthropogenic effects on prey traits are multi-faceted and often not mutually-exclusive including through climate change (Bastille-Rousseau et al. 2018, Gallagher 2022), exploitation of prey (Bonnet et al. 2021, Darimont et al. 2009, Dulvy et al. 2004), introduction of invasive prey (Cattau et al. 2018, Phillips and Shine 2004, Queral-Regil and King 1998, Steinhardt et al. 2004), and habitat alteration (Evans et al. 2022, Farias and Kittlein 2008, Schneider 2001).

This study utilizes another example of an anthropogenic shift on prey through landscape change, agriculture. In the mid-1900’s, Arkansas became a leader in fish aquaculture, developing dozens of fish farms throughout the Mississippi Floodplain (Engle et al 2021, Freeze and Scott 1979, Feigel and Freeze 1981, Meyer et al. 1970). Notably, these farms vary extensively in the species and size of fish cultured. Consequently, diamond-backed watersnakes (Nerodia rhombifer), a fish-specialist predator that naturally colonized these newly constructed farms, experienced highly variable prey sizes among populations. Over the last twelve years, studies have clearly demonstrated substantial differences in many aspects of the life-history of these snakes including adult body size that correlate with the average size of fish prey produced at each site (Korfel et al. 2015; Clifton et al. 2017; Chamberlain et al. 2017; Clifton et al. 2020; Chamberlain 2016). Surprisingly, these clear body size patterns have emerged over a relatively short time period. This begs the question of what mechanism is driving these responses. Is it a genetic response to natural selection or phenotypic plasticity? A growing body of literature suggests that while long-term responses of phenotypes to novel selective pressures may stem from genetic adaptation, phenotypic plasticity may be an initial mechanism permitting initial colonization. Individuals within a species may persist in a novel habitat, particularly those stemming from anthropogenic change, by favorably shifting their phenotype non-heritably (Aubret 2015, Aubret and Shine 2009, Bonnet et al 2021, Clifton et al 2020, Ghalambhor et al. 2007). In snakes, the general pattern of response appears to be shaped mostly by phenotypic plasticity, however that is not always the case (see Bonnet et al. 2021, but also Bronikowski 2000, Forsman and Shine 1997). To fully understand the long-term responses of wildlife populations to human-induced change, it is necessary to determine the nature of these mechanisms shaping phenotypes.

Since adult body size differences are strongly influenced by variation in initial offspring size and juvenile growth rate, these traits are clear phenotypic targets for testing plastic or genetic responses to selection of prey size (Falster et al. 2008, Dmitriew 2011, Sinervo 1993, Taborsky 2006, Uller and Olsson 2010). Among the fish farm populations of watersnakes we have measured, there are strong differences in initial offspring size that also correlate with prey size consistent with patterns of adult size (Chamberlain et al 2017).

The focus of this study was to assess the influence of plasticity or genetic adaption of juvenile growth rate among these populations of snakes as possible mechanisms driving the observed differences in adult body sizes. Using a common-garden design, we measured the growth rates of neonate diamond-backed watersnakes from three populations that vary in average prey size and adult body sizes. This design also allows us to test the influence of initial offspring size on juvenile growth rates. We hypothesized that if growth rates among populations differed in the lab after controlling for the effect of the mass of fish consumed during the experiment, then they are the result of genetic adaptation. Alternatively, if growth rates among populations only differed before accounting for mass of prey consumed, then the differences are largely the result of phenotypic plasticity. Lastly, if we detected no differences in growth rate among populations even before correcting for mass of prey consumed, then differences in adult body sizes among fish farms are likely the product of initial offspring size.

Study sites:

We selected three fish farms in Lonoke County, Arkansas, United States because of their historical differences in the fish species cultivated. We describe these populations more thoroughly elsewhere, as they are a part of an on-going mark-recapture study focusing on exploring life-history variation among these populations (Korfel et al. 2015; Clifton et al. 2017; Chamberlain et al. 2017; Clifton et al. 2020; Chamberlain 2016). These farms are characterized by a highly altered but stable environment, providing resident snakes with a constant, dense source of fish prey throughout the active season. However, these farms differ substantially in the average size of fish raised. Two farms are characterized by large average fish sizes, and one farm characterized by small fish. The first of the two large-prey sites, Keo Fish Farm LLC (KEO), was established in 1986, and specializes in the production of triploid grass carp (Ctenopharyngodon idealla) and hybrid striped bass (Morone saxitilis/chrysops). The other large-prey site, Joe Hogan State Fish Hatchery (JOHO), was established in the 1950’s, and produces several warm-water fish species including largemouth bass (Micropterus salmoides) and black crappie (Pomoxis nigromaculatus), but 80% of their production is channel catfish (Ictalurus punctatus). Gentry and Canterberry Fisheries LLC (GNC) represents the small-prey site and specializes in production of goldfish (Carassius auratus) for the pet trade and fishing industries.

We have characterized body size differences of the watersnakes colonizing these sites. Female snakes from large-prey sites (KEO and JOHO) have an 8% larger maximal adult body length than their conspecifics from the small-prey site (GNC) (Clifton et al. 2017). Interestingly, adult male body sizes among these populations do not differ. This species shows substantial female-larger sexual size dimorphism with females likely experiencing a fecundity advantage with larger body sizes (Mushinsky et al. 1982, Shine 1988, Shine 2003). Initial body size at birth also differs among these populations. Snakes from large prey sites produce offspring that are on average 4.5% longer and 23% heavier than those at small prey sites (Chamberlain et al. 2017).

Common-garden laboratory growth rates:

We collected pregnant females from each site in July of 2013 (n = 11, 8, and 10 for JOHO, KEO, and GNC, respectively) and allowed them to give birth in the laboratory as part of a larger reproduction study (Chamberlain 2016, Chap. 2). Parturition dates ranged from 23 August to 1 October. Six neonates, 3 male and 3 female, from each litter were randomly selected for inclusion in the growth study. We marked and released all remaining neonates from each litter to their native populations. We only used individuals that survived the duration of the study in subsequent analyses. With 11 individuals removed due to mortality, the total number of individuals used in analyses was 168 neonates (n = 66, 45, and 57 from JOHO, KEO, and GNC, respectively).

Each neonate was individually housed within a rack system (Vision Products, Canoga Park, CA) and provided aspen bedding and continual access to water. The rack system enclosures (46 cm x 13 cm x 9 cm) provided a thermal gradient ranging from 25 to 31°C by including a heating element under the rear third of each tub. We estimated total weekly consumption of each snake as a covariate in growth rate analyses. Snakes were fed live fathead minnows (Pimephales promelas) weekly. Fish were placed in the water bowl of each snake in the evening and uneaten fish were removed and counted the following morning. The mass of fish consumed was estimated as the average mass of one fish multiplied by the number of fish eaten. The number of fish provided to each snake was counted at each feeding. Average weight of each fish was estimated as the average mass of a subsample of 10 fish from each weekly feeding. The number of fish provided each week was the maximum number of fish eaten the previous week by any individual snake plus one. Snakes initially fed 1–2 weeks after birth, often before the beginning of the common garden growth experiment. Thus, we only calculated the total mass of fish consumed during the actual growth experiment for use as a covariate. The mass of fish consumed was handled one of two ways depending on the analysis. We either calculated the total mass of fish consumed over the entire duration of the study as a single value (Total Consumption) or we added each week’s consumption to the total mass of fish consumed from the beginning of the study to that point (Cumulative Weekly Consumption).

We measured snout-vent length (SVL) of all neonates at birth and again at the beginning of the experiment using a standard meter stick, measuring to the nearest 0.1 cm. While there was variability in the timing of parturition among females both within and among populations, the average age of neonates at the start of the experiment did not significantly differ among the populations after the Tukey test for pairwise comparisons (F_2,26 = 3.367, p = 0.050, GNC-JOHO: p = 0.0718, GNC-KEO: p = 0.900, KEO-JOHO: p = 0.112). GNC and KEO snakes were on average 21 days old at the start of the experiment and JOHO neonates were 31 days old). The growth experiment began on 23 August, 2013 and finished 31 January, 2014. During the study, we measured SVL every two weeks over the course of the 161-day experiment.

Statistical Analysis:

We compared the initial size at birth and total consumption among populations using a mixed effects model ANOVA with Satterthwaite’s Type III sums of squares (R: lme4 package, Bates et al. 2015). In these analyses, we fitted population as a fixed effect and mother as a random effect (to account for non-independence due to sibship). We determined population differences using Tukey corrections for pairwise comparisons (R: emmeans package, Lenth 2016). We estimated growth rate among populations statistically by extracting the slopes of the linear mixed effects model where SVL was the response variable, age and population were fixed effects, and mother and individual were random effects (R: emmeans package, Lenth 2016). The presence of significant differences in growth rate was confirmed by an age*population interaction. Pairwise differences in these growth rate slopes among populations were compared using a Tukey correction (R: emmeans package, Lenth 2016). This same model was repeated, including cumulative weekly consumption as an additional fixed effect to estimate its relative effect on resulting growth rate differences. Additionally, we regressed the extracted growth rate values for each individual from the linear mixed effects model with total consumption using a linear mixed effects model with total consumption and population as fixed effects, and mother as a random effect. Because of the presence of a significant interaction between the fixed effects in this model, we measured the population pairwise comparisons of the slopes using a Tukey correction. We used this test as a measure of growth efficiency, looking at the proportion of length gained per unit of prey mass consumed.

To test the relationship between initial offspring size and total consumption, we ran a linear mixed effects model using total consumption as a response variable, initial SVL at birth and population as fixed effects, and mother as a random effect. We used this model to examine if populations differed in proportion of prey consumed at any given size.

While sex was included in the all the above models as a fixed effect, the only time we detected a significant effect of sex was in the comparison of growth rates. Therefore we omit F-statistics for sex as a factor in subsequent analyses except those associated with initial offspring size and growth rate models. All averages are reported as the mean ± standard error.

Initial length at birth differed among populations as expected (Fig. 1; F_{2, 28}= 3.803, p = 0.034). Neonates from JOHO (25.8 ± 0.3 cm) were significantly larger than those from GNC (24.7 ± 0.3 cm), but KEO (25.2 ± 0.4 cm) did not differ from either JOHO or GNC. Neonates also significantly differed in SVL at the beginning of the growth experiment (F_{2, 28}= 4.434, p = 0.021) reflecting the same pattern as the differences at birth, with JOHO and GNC significantly differing, but GNC and KEO not differing, and likewise for KEO and JOHO. The initial size of offspring did not differ between sexes within or among any of the populations (Sex: F_1,135 = 0.0956, p = 0.758; Sex*Population: F_2,135 = 0.2401, p = 0.787).

Over the duration of the study, neonates from JOHO (90.8 ± 5.5 g) ate a significantly larger total mass of fish compared to GNC (70.7 ± 5.8 g), and KEO (82.3 ± 6.5 g) did not differ from either JOHO or GNC in the total mass of fish consumed (Fig. 2; F_2,29 = 3.518, p = 0.043). There was a significant relationship between the initial size of offspring and the total mass of fish consumed during the trial that did not differ among populations (Fig. 3; Initial SVL: F_1,110 = 5.898, p = 0.017; Population: F_2,108 = 0.974, p = 0.381; SVL*Population: F_2,108 = 1.155, p = 0.319). Within all populations, larger neonates ate a larger mass of fish over the course of the study than their small counterparts, and the slope of this relationship did not differ among the populations. Neonates of similar size across all populations ate similar amounts of fish over the course of the study.

When growth rate was estimated without accounting for cumulative weekly consumption in the model, both JOHO and KEO snakes had significantly faster growth rates than GNC snakes, but did not differ from each other (Fig. 4; Age*Population: F_2,1503 = 11.074, p < 0.001; GNC-JOHO: T₁₅₀₅ = -3.838, p < 0.001; GNC-KEO: T₁₅₀₆ = -4.257, p < 0.001; JOHO-KEO: T₁₅₀₆ = -0.879, p = 0.654). When cumulative weekly consumption was added to the model as a fixed effect we were no longer able to detect an age*population interaction, suggesting there is no difference in growth rate among populations after accounting for population-level differences in the amount of fish they consumed over that same period of time (Age*Population: F_2,1624 = 1.151, p = 0.220). The pattern is different for sex, however. We found a significant age*sex interaction (Fig. 5; Age*Sex: F_1,1641 = 12.608, p < 0.001) with females having a slightly faster growth rate than males. Further, when cumulative weekly consumption was added to the model, we still detected this difference in growth rate (Age*Sex: F_1,1641 = 11.695, p < 0.001), unlike the pattern of growth rates among populations. We did not, however, detect an age*sex*population interaction (Age*Sex*Population: F_2,1641 = 0.995, p = 0.370) in a model excluding cumulative weekly consumption. This suggests that when growth rate is compared among females and males from all populations combined, we detected a difference in growth rate, but that there is no difference between the sexes among any of the sites.

The growth rate estimates extracted from the slopes of the model above that excluded cumulative weekly consumption and sex were also regressed with total consumption over the course of the study. There is a strongly significant positive relationship between total consumption and growth rate (Fig. 6; F_1,159 = 415.796, p < 0.001). This model also shows a significant interaction between total consumption and population (F_2,153 = 3.373, p = 0.037). Again, total consumption scales with growth rate marginally faster at GNC than at JOHO (GNC-JOHO: T₁₇₁ = 2.316, p = 0.056), but not significantly so with KEO (GNC-KEO: T₁₇₄ = 0.541, p = 0.851). Total consumption and growth rate scale similarly at KEO and JOHO (JOHO-KEO: T₁₅₉ = -1.649, p = 0.229). Using this measure as an estimate of growth efficiency, our data suggest that snakes from GNC grows proportionally faster for the mass of prey consumed than the other two populations.

Our data support the growing consensus of literature, particularly for snakes, that rapid shifts in adult morphology across populations are frequently the product of plasticity in growth during ontogeny (Aubret 2012, Aubret 2015, Aubret et al. 2004, Aubret and Shine 2007, Aubret and Shine 2009, Aubret and Shine 2010, Bonnet et al. 2001, Bonnet et al. 2021, Brown et al 2017, Forsman 2015, Ghalambor et al. 2007, Madsen and Shine 1993, Pigliucci et al. 2006, Queral-Regil and King 1998, Stearns 1989). Here, we demonstrate that neonates from populations of diamond-backed watersnakes that have access to larger average prey sizes (KEO and JOHO) have larger initial body sizes and proportionally faster growth rates than neonates from a population with access to smaller average prey sizes (GNC). Differences in the average growth rate among these populations are only detected before correcting for mass of prey consumed. Once corrected, we were unable to detect any population-level differences in growth rate. These analyses suggest that the major driver of differences in growth rate is the mass of prey consumed. We, therefore, suggest that growth rate is a plastic response of initial size and the ability of larger individuals to consume more prey mass in a given amount time than their smaller counterparts over the same period. This idea is supported by our finding that across all populations the total mass of prey consumed was strongly correlated with the initial size of offspring, and scaled similarly among all populations.

If we interpret the results of this experiment in the context of the populations in the field, then larger adult sizes seen at JOHO and KEO likely are the result of females at these sites producing larger initial offspring sizes. These larger initial body sizes drive faster growth rates by allowing individuals to consume greater masses of prey over time. This same relationship likely exists within each of the three populations as well. The largest neonates within each population should also have the fastest growth rates. Interestingly, our data support Marshall et al. (2018) in their hypothesis that larger initial offspring sizes should be favored when the larger body sizes allowed neonates to disproportionately gain more calories to offset the energetic cost of maintaining a larger body size. This finding parallels those from a previous study of these watersnake populations (Clifton et al. 2020). While examining plasticity of trophic morphology in response to differing prey sizes, the authors found that the larger-bodied neonates from large-prey sites were more successful in handling larger prey earlier, resulting in more rapid growth than neonates from small-prey sites. Taken together, these two studies suggest that faster growth rates are the product of increased energetic processing and not simply a response to prey abundance or prey size exclusively. Both traits resulted in the same pattern of growth rate between the two studies.

Life-history and body morphology patterns of snakes on these fish farms highlight an important but likely unintended consequence of anthropogenic change on the landscape. Highly localized changes to the environmental landscape result in increased inter-population variance of morphology and physiology in wildlife populations, often with unknown consequences. The role phenotypic plasticity plays in the sustainability, resiliency and rate of response to rapid environmental change is quickly becoming of a major focus of evolutionary and ecological research (Bonnet et al. 2021, Charmantier et al. 2008, Fox et al 2018, Norin and Metcalfe 2019, Scheiner et al. 2019, Torda et al 2017). What makes this system unique and an interesting model for studying the long-term consequences of phenotypic plasticity is the fine-scale level of this variation and the fact these differences are maintained across generations in the face of what is likely a high level of gene flow. Of the more 2,000 km² of land in Lonoke County, AR, 8% of the land mass is dedicated to fish farming as of 2017, resulting in a dense patchwork of fish farms across the landscape (2017 Census of Agriculture Report, USDA). The fish farms used in this study were no more than 3 km from the nearest neighboring fish farm. Most fish farms within the county cultivate different species of fish and/or raise fish to different sizes, resulting in a complicated matrix of prey-related selective pressures spaced closely together. Additionally, most of these farms are connected by a network of canals, drainage ditches, and natural waterways, providing a potential route of migration from one farm to the next for these highly aquatic snakes.

It should also be noted that although KEO neonates were not significantly larger at birth (25.2 ± 0.4 cm) nor did they eat significantly more prey items (82.3 ± 6.5 g) than neonates from the small prey population GNC (24.7 ± 0.3 cm; 70.7 ± 5.8 g) (Fig. 2 & Fig. 3), the neonates from KEO grew significantly faster than those from GNC (Fig. 4). This may simply be a function of the smaller than average body size of KEO neonates in this study, but may provide some evidence for underlying genetic selection for faster growth at this site. Interestingly, while GNC may have slower growth rates than either KEO or JOHO, their growth efficiency is higher (Fig. 5). These data suggest that neonates from GNC put on disproportionally more length for each gram of fish consumed than those from either of the large prey sites. The mechanism or importance of this relationship is unclear, and further work is required for interpretation.

While faster growth rates may be an indirect consequence of larger initial body sizes among populations, it is still unclear if variation in initial body size among populations is the product of selective pressure of prey size on neonates or the non-adaptive result of increased maternal investment in populations where females reach larger body sizes. Female body size is strongly correlated with offspring size in this species (Chamberlain et al. 2017). It is surprising that very little work has been done to understand the relationship between average prey size and average initial offspring size in snakes, given the fact that they are gape-limited predators. One notable exception is work of Aubret (2012) on populations of insular tiger snakes that exhibit gigantism and dwarfism. In that paper, he argues that adult body size differences among populations are the consequence of strong selection on initial offspring size to consume larger prey. On islands where the average prey size was large, populations of tiger snakes produce large offspring while the opposite is true on islands with small prey.

The sex differences we detected in growth rate align with predictions of sexual size dimorphism in this species. Adult female body sizes are significantly larger at large prey populations (JOHO and KEO) compared to females from small prey populations (GNC). Adult male body sizes, however, do not significantly differ among the populations. Across all populations, adult female body size is larger than adult males (Clifton et al. 2017), likely stemming from the faster female juvenile growth rates we detected compared to males. Adult female watersnakes likely experience a “fecundity-advantage” with increasing body size (Shine 1988; Weatherhead et al. 1995). Therefore, prey size selection on body size should remain throughout ontogeny. On the other hand, in watersnakes and other natricid snakes, smaller adult male sizes are often favored (Brown and Weatherhead 1999; Rivas and Burghardt 2001; Weatherhead et al. 1995). If larger prey are available, larger adult female body sizes should be favored because of the increased caloric intake and the resulting increases to reproductive output, not necessarily so for males. It is important to note, that while the differences among populations for growth rate seem to be the product of phenotypic plasticity driven by variation in consumption of prey at larger sizes, sex differences in growth rate are not explained by either the amount of prey consumed or by the initial size difference as we still detected significant differences after controlling for these factors. Sex differences in growth rate resulting in sexual size dimorphism is widespread phenomenon, particularly in ectothermic and gape-limited predators. However, the regulatory underpinnings of these differences can vary substantially. Many researchers have detected sexual size dimorphism as a product of phenotypic plasticity (Brown et al 2017, Fernandez-Montraveta and Moya-Larano 2007, Haenel and John-Alder 2002, Luiselli et al. 2002, Madsen and Shine 1993, Rhen 2007), while others have demonstrated that canalization of these differences between sexes are maintained genetically (Badyaev et al. 2000, Lande 1980, Le Galliard et al. 2006, Rhen 2007, Stillwell and Fox 2009). Regardless of the source, these differences are likely mediated through sex-specific differences in hormonal expression and regulation (Cox and John-Alder 2005, Cox and John-Alder 2007, Cox et al. 2017, Cox et al. 2022). Further studies are needed to isolate the genetic vs. plastic components of the detected differences in growth rate between sexes in this study.

The results of this experiment provide evidence that support the growing body of literature that adaptive plasticity may be a primary driver of rapid phenotypic divergence among populations across a landscape. This mechanism may explain the stability and colonization of wild populations in the face of rapid, human-mediated, landscape changes. This experiment also illustrates the relationship between initial offspring size and juvenile growth rate in gape-limited predators. We propose that larger offspring sizes may favor increased growth rates, mediated through a larger energy processing capacity relative to smaller individuals.

Acknowledgements

We thank A. Anderson, T. Clay, C. Korfel, M. Pollett, A. Winters, and numerous other volunteers for their assistance in collecting and housing snakes. Additionally, we thank Gentry and Canterberry Fisheries LLC, Keo Fish Farm, and Arkansas Game and Fish Commission for generously allowing us to sample their properties. We also thank R. Sikes, W. Baltosser, D. Jones, and J.D. Willson for reviewing this manuscript. Finally, we thank the Basic Animal Services Unit at the University of Arkansas at Little Rock for allowing use of their facilities.

Funding: Not Applicable

Conflict of Interests: The authors declare that they have no conflict of interest.

Ethics Approval: This project was covered under University of Arkansas at Little Rock Institutional Animal Care protocol R-12-03 and Arkansas Game and Fish permit #031220131. All field and laboratory use of animals followed the American Society of Ichthyologists and Herpetologists guidelines for use of live reptiles in research (Beaupre et al. 2004)

Consent to Participate: Not applicable

Consent for Publication: Not applicable

Availability of Data: The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Code Availability: All R-script code used for statistical analysis are available from the corresponding author on reasonable request.

Authors Contributions: JDC, ITC and MEG conceived and designed the experiments, performed the experiments, analyzed the data, and wrote the manuscript.

Aarssen LW (2015) Body size and fitness in plants: Revisiting the selection consequences of competition. Perspect Plant Ecol 17:236–242. https://doi.org/10.1016/j.ppees.2015.02.004
Ashton KG (2004) Sensitivity of intraspecific latitudinal clines of body size for tetrapods to sampling, latitude, and body size. Integr Comp Biol 44:403–412.
Aubret F (2012) Body-size evolution on islands: Are adult size variations in Tiger Snakes a nonadaptive consequence of selection on birth size. Am Nat 179:756–767. https://doi.org/10.1086/665653
Aubret F (2015) Island colonisation and the evolutionary rates of body size in insular neonate snakes. Heredity 115:349–356. https://doi.org/10.1038/hdy.2014.65
Aubret F, Shine R (2007) Rapid prey-induced shift in body size in an isolated snake population (Notechis scutatus, Elapidae). Austral Ecol 32:889–899. https://doi.org/10.1111/j.1442-9993.2007.01777.x
Aubret F, Shine R (2009) Genetic assimilation and the post-colonization erosion of phenotypic plasticity in Island Tiger Snakes. Curr Biol 19:1932–1936. https://doi.org/10.1016/j.cub.2009.09.061
Aubret F, Shine R (2010) Fitness costs may explain the post-colonisation erosion of phenotypic plasticity. J Exp Biol 213:735–739. https://doi.org/10.1242/jeb.040576
Bastille-Rousseau G, Schaefer JA, Peers MJL, Ellington EH, Mumma MA, Rayl ND, Mahoney SP, Murray DL (2018) Climate change can alter predator – prey dynamics and population viability of prey. Oecologia 186:141–150. https://doi.org/10.1007/s00442-017-4017-y
Badyaev AV, Hill GE, Stoehr AM, Nolan PM, McGraw KJ (2000) The evolution of sexual size dimorphism in the house finch. II. Population divergence in relation to local selection. Evolution 54:2134–2144.
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models Using lme4. J Stat Softw 67:1–48. doi:10.18637/jss.v067.i01.
Beaupre SJ, Jacobson R, Lillywhite H, Zamudio KR (2004) Guidelines for use of live amphibians and reptiles in field and laboratory research. American Society of Ichthyologists and Herpetologists. https://doi.org/http://iacuc.ucsd.edu/PDF_References/ASIH-HL-SSAR%20Guidelines%20for%20Use%20of%20Live%20Amphibians%20and%20Reptiles.htm
Blanckenhorn WU (2000) The evolution of body size: What keeps organisms small? Q Rev Biol 75: 385–407.
Blumenshine SC, Lodge DM, Hodgson JR (2000) Gradient of fish predation alters body size distributions of lake benthos. Ecology 81: 374–386.
Boback SM (2003) Body size evolution in snakes: Evidence from island populations. Copeia 2003: 81–94.
Bonnet X, Shine R, Naulleau G, Thiburce C (2001) Plastic vipers: influence of food intake on the size and shape of Gaboon vipers (Bitis gabonica). J Zool 255: 341–351.
Bonnet X, Brischoux F, Briand M, Shine R, Bonnet X (2021) Plasticity matches phenotype to local conditions despite genetic homogeneity across 13 snake populations. Proc R Soc B-Biol Sci 288: 1–8.
Bronikowski AM (2000) Experimental evidence for the adaptive evolution of growth rate in the garter snake Thamnophis elegans. Evolution 54: 1760–1767.
Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150: 28–35.
Brown GP, Weatherhead PJ (1999) Demography and sexual size dimorphism in northern water snakes, Nerodia sipedon. Can J Zool 77: 1358–1366. https://doi.org/10.1139/cjz-77-9-1358
Brown GP, Madsen TRL, Shine R (2017) Resource availability and sexual size dimorphism: differential effects of prey abundance on the growth rates of tropical snakes. Funct Ecol 31: 1592–1599. https://doi.org/10.1111/1365-2435.12877
Cattau CE, Fletcher Jr RJ, Kimball RT, Miller CW, Kitchens WM (2018) Rapid morphological change of a top predator with the invasion of a novel prey. Nat Ecol Evol 2: 108–115. https://doi.org/10.1038/s41559-017-0378-1
Chamberlain JD (2016) Life-history and energetics of the diamond-backed watersnake. PhD Dissertation, Department of Applied Bioscience, Univeristy of Arkansas at Little Rock, Little Rock, Arkansas, USA.
Chamberlain JD, Clifton IT, Gifford ME (2017) Influence of prey size on reproduction among populations of diamond-backed watersnakes (Nerodia rhombifer). Can J Zool 935: 929–935. https://doi.org/10.1139/cjz-2017-0002
Clifton IT, Chamberlain JD, Gifford ME (2017) Patterns of morphological variation following colonization of a novel prey environment. J Zool 302: 263–270. https://doi.org/10.1111/jzo.12459
Clifton IT, Chamberlain JD, Gifford ME (2020) Role of phenotypic plasticity in morphological differentiation between watersnake populations. Integr Zool 15: 329–337. https://doi.org/10.1111/1749-4877.12431
Cox RM, Cox CL, McGlothlin JW, Card DC, Andrew AL, Castoe TA (2017) Hormonally mediated increases in sex-biased gene expression accompany the breakdown of between-sex genetic correlations in a sexually dimorphic lizard. Am Nat 189:315–332. https://doi.org/10.1086/690105
Cox RM, John-Alder HB (2005) Testosterone has opposite effects on male growth in lizards (Sceloporus spp.) with opposite patterns of sexual size dimorphism. J Exp Biol 208: 4679–4687. https://doi.org/10.1242/jeb.01948
Cox RM, John-Alder HB (2007) Growing apart together: The development of contrasting sexual size dimorphisms in sympatric Sceloporus lizards. Herpetologica 63: 245–257. https://doi.org/10.1655/0018-0831(2007)63[245:GATTDO]2.0.CO;2
Cox CL, Logan ML, Nicholson DJ, Chung AK, Rosso AA, Mcmillan WO, Cox RM (2022) Species-specific expression of growth-regulatory genes in 2 anoles with divergent patterns of sexual size dimorphism. Integr Org Biol 4: 1–13. https://doi.org/10.1093/iob/obac025
Darimont CT, Carlson SM, Kinnison MT, Paquet PC, Reimchen TE, Wilmers CC (2009) Human predators outpace other agents of trait change in the wild. Proc Natl Acad Sci USA 106: 952–954.
De Jong G, Imasheva A (2001) Genetic variance in temperature dependent adult size deriving from physiological genetic variation at temperature boundaries. Genetica 110: 195–207.
Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86: 97–116. https://doi.org/10.1111/j.1469-185X.2010.00136.x
Dulvy NK, Freckleton RP, Polunin NVC (2004) Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol Lett 7:410–416. https://doi.org/10.1111/j.1461-0248.2004.00593.x
Engle CR, Hanson T, Kumar G (2021) Economic history of U.S. catfish farming: Lessons for growth and development of aquaculture. Aquacult Econ Manag 26: 1–35. https://doi.org/10.1080/13657305.2021.1896606
Evans BA, Klassen JA, Gawlik DE (202) Dietary flexibility of wood storks in response to human-induced rapid environmental change. Urban Ecosyst 25: 705-715. https://doi.org/https://doi.org/10.1007/s11252-021-01181-9
Falster DS, Moles AT, Westoby M (2008) A general model for the scaling of offspring size and adult size. Am Nat 172:299–317. https://doi.org/10.1086/589889
Farias AA, Kittlein MJ (2008). Small-scale spatial variability in the diet of pampas foxes (Pseudalopex gymnocercus ) and human-induced changes in prey base. Ecol Res 23: 543–550. https://doi.org/10.1007/s11284-007-0407-7
Fernandez-Montraveta C, Moya-Larano J (2007) Sex-specific plasticity of growth and maturation size in a spider: Implications for sexual size dimorphism. J Exp Biol 20: 1689–1699. https://doi.org/10.1111/j.1420-9101.2007.01399.x
Fiegel DH, Freeze M (1981) Aquaculture industry of Arkansas in 1979-1980. J Ark Acad Sci 35: 40–42.
Forsman A (1991) Variation in sexual size dimorphism and maximum body size among adder populations: Effects of prey size. J Anim Ecol 60: 253–267.
Forsman A (1996) Body size and net energy gain in gape-limited predators: A model. J Herpetol 30: 307–319.
Forsman A (2015) Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity 115:276–284. https://doi.org/10.1038/hdy.2014.92
Forsman A, Shine R (1997) Rejection of non-adaptive hypotheses for intraspecific variation in trophic morphology in gape-limited predators. Biol J Linn Soc 62: 209–223. https://doi.org/Doi 10.1111/J.1095-8312.1997.Tb01623.X
Freeze M, Henderson S (1979) The aquaculture industry of Arkansas in 1979. Proc Ann Conf S Assoc Fish Wild Agen 34: 115–126.
Gallagher CA, Chimienti M, Grimm V, Nabe-Nielsen J (2022) Energy-mediated responses to changing prey size and distribution in a marine top predator movements and population dynamics. J Anim Ecol 91: 241-254. https://doi.org/10.1111/1365-2656.13627
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21: 394–407. https://doi.org/10.1111/j.1365-2435.2007.01283.x
Haenel GJ, John-Alder HB (2002) Experimental and demographic analyses of growth rate and sexual size dimorphism in a lizard, Sceloporus undulatus. Oikos 96: 70–81.
Jessop TS, Madsen T, Sumner J, Rudiharto H, Phillips JA, Ciofi C (2006) Maximum body size among insular Komodo dragon populations covaries with large prey density. Oikos 112: 422–429.
Keogh JS, Scott IAW, Hayes C (2005) Rapid and repeated origin of insular gigantism and dwarfism in Australian Tiger Snakes. Evolution 59: 226–233.
King RB, Ray JM, Stanford KM (2006) Gorging on gobies: beneficial effects of alien prey on a threatened vertebrate. Can J Zool 84: 108–115. https://doi.org/10.1139/z05-182
King RB, Hampton PM, Altman KA, Paull SH, Johnson PTJ, Golembieski MN, Stephens JP, Lafonte BE, Raffel TR (2016) Predicted and observed maximum prey size - Snake size allometry. Funct Ecol 217: 1014–1024. https://doi.org/10.1242/jeb.092924
Korfel CA, Chamberlain JD, Gifford ME (2015) A test of energetic trade-offs between growth and immune function in watersnakes. Oecologia 179: 343–351. https://doi.org/10.1007/s00442-015-3365-8
LaBarbera M (1989) Analyzing body size as a factor in ecology and evolution. Annu Rev Ecol Syst 20: 97–117.
Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34: 292–305.
Le Galliard J-F, Massot M, Landys MM, Meylan S, Clobert J (2006) Ontogenic sources of variation in sexual size dimorphism in a viviparous lizard. J Evol Biol 19: 690–704. https://doi.org/10.1111/j.1420-9101.2006.01094.x
Lenth RV (2016) Least-Squares Means: The R Package lsmeans. J Stat Softw 69: 1–33. doi:10.18637/jss.v069.i01.
Lindmark M, Huss M, Ohlberger J, Gardmark A (2018) Temperature-dependent body size effects determine population responses to climate warming. Ecol Lett 21: 181–189. https://doi.org/10.1111/ele.12880
Luiselli LM, Akani GC, Godfrey C, Corti C, Francesco M (2002) Is sexual size dimorphism in relative head size correlated with intersexual dietary divergence in West African forest cobras , Naja melanoleuca? Contrib Zool 71: 141–145.
Madsen TRL, Shine R (1993) Phenotypic plasticity in body sizes and sexual size dimorphism in European grass snakes. Evolution 47: 321–325.
Madsen TRL, Shine R (2000) Silver spoons and snake body sizes: Prey availability early in life influences long-term growth rates of free-ranging pythons. J Anim Ecol 69: 952–958.
Marshall DJ, Pettersen AK, Cameron H (2018) A global synthesis of offspring size variation, its eco-evolutionary causes and consequences. Funct Ecol 32: 1436–1446. https://doi.org/10.1111/1365-2435.13099
Meyer FP, Godwin DS, Boyd R, Martini JM, Gray DL, Mathis WP (1970) Fish production in Arkansas during 1969 as compared to other states. Proc Annu Conf S Assoc Game Fish Comm 24: 497–506.
Mushinsky HR, Hebrard JJ, Vodopich DS (1982) Ontogeny of water snake foraging ecology. Ecology 63: 1624–1629.
Palkovacs, EP (2003) Explaining adaptive shifts in body size on islands: A life history approach. Oikos 103: 37–44.
Phillips BL, Shine R (2004) Adapting to an invasive species: Toxic cane toads induce morphological change in Australian snakes. Proc Natl Acad Sci USA 101: 17150–17155. https://doi.org/10.1073/pnas.0406440101
Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209: 2362–2367. https://doi.org/10.1242/jeb.02070
Rhen T (2007) Sex differences: genetic, physiological, and ecological mechanisms. In: Fairbairn DJ, Blanckenhorn WU, Szekely T (eds) Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism, Oxford University Press, Oxford. pp 167–175.
Rivas SA, Burghardt GM (2001) Understanding sexual size dimorphism in snakes: wearing the snake’s shoes. Anim Behav 62: F1–F6. https://doi.org/10.1006/anbe.2001.1755
Roff DA (1992) Evolution of life histories: Theory and analysis. Chapman and Hall, New York
Queral-Regil A, King RB (1998) Evidence for phenotypic plasticity in snake body size and relative head dimensions in response to amount and size of prey. Copeia 1998: 423–429.
Scharf FS, Juanes F, Rountree RA (2000) Predator size - prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208: 229–248.
Schneider MF (2001) Habitat loss, fragmentation and predator impact: spatial implications of prey conservation. J Appl Ecol 38: 720–735.
Sears MW, Angilletta MJ (2004) Body size clines in sceloporus lizards: proximate mechanisms and demographic constraints. Integr Comp Biol 44:433–442. https://doi.org/10.1093/icb/44.6.433
Shine R (1988) The evolution of large body size in females: A critique of Darwin’s “Fecundity Advantage” model. Am Nat 131:124–131.
Shine R (2003) Reproductive strategies in snakes. Proc R Soc B-Biol Sci 270: 995–1004. https://doi.org/10.1098/rspb.2002.2307
Sinervo B (1993) The effect of offspring size on physiology and life history. Bioscience 43: 210–218.
Smith JM, Brown RLW (1986) Competition and body size. Theor Popul Biol 30: 166–179.
Stearns SC (1989) The evolutionary significance of plasticity. Biocience 39: 436–445.
Stearns SC (1992) The evolution of life histories. Oxford University Press, New York.
Steinhart GB, Stein RA, Marschall EA (2004) High growth rate of young-of-the-year smallmouth bass in Lake Erie: A result of the round goby invasion. J Great Lakes Res 30: 381–389. https://doi.org/10.1016/S0380-1330(04)70355-X
Stillwell RC (2010) Are latitudinal clines in body size adaptive? Oikos 119: 1387–1390. https://doi.org/10.1111/j.1600-0706.2010.18670.x.
Stillwell RC, Fox CW (2009) Geographic variation in body size , sexual size dimorphism and fitness components of a seed beetle: local adaptation versus phenotypic plasticity. Oikos 118: 703–712. https://doi.org/10.1111/j.1600-0706.2008.17327.x
Sun L, Shine R, Zhao D, Tang Z (2002) Low costs, high output: reproduction in an insular pit-viper (Gloydius shedaoensis, Viperidae) from north-eastern China. J Zool 256: 511–521. https://doi.org/10.1017/S0952836902000560
Taborsky B (2006) The influence of juvenile and adult environments on life-history trajectories. Proc R Soc B-Biol Sci 273: 741–750. https://doi.org/10.1098/rspb.2005.3347
Tibblin P, Forsman A, Koch-Schmidt P, Nordahl O, Johannessen P, Nilsson J, Larsson P (2015) Evolutionary divergence of adult body size and juvenile growth in sympatric subpopulations of a top predator in aquatic ecosystems. Am Nat 186:98–110. https://doi.org/10.1086/681597
Uller T, Olsson M (2010) Offspring size and timing of hatching determine survival and reproduction output in a lizard. Oecologia 162: 663–671. https://doi.org/10.1007/S00442-009-1503-X
Weatherhead PJ, Barry FE, Brown GP, Forbes MRL (1995) Sex ratios, mating behavior and sexual size dimorphism of the northern water snake, Nerodia sipedon. Behav Ecol Sociobiol 36: 301–311.

Download PDF

Journal Publication

published 20 Sep, 2024

Read the published version in Oecologia →

Reviewers agreed at journal
30 Aug, 2023
Reviewers invited by journal
29 Aug, 2023
Editor assigned by journal
28 Jul, 2023
First submitted to journal
26 Jul, 2023

You are reading this latest preprint version

Plastic juvenile growth rates and offspring size: A response to anthropogenic shifts in prey size among populations

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Methods

Study sites:

Common-garden laboratory growth rates:

Statistical Analysis:

Results

Discussion

Declarations

References

Status:

Journal Publication

Version 1