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Eco-evolutionary dynamics occur when ecological change influences evolutionary change (eco-to-evo) and when evolutionary change influences ecological change (evo-to-eco), both on contemporary time scales. Fishes, amphibians, and reptiles have played important roles as study animals in the empirical study and exploration of these dynamics. We suggest that this primacy stems in part from the sweet-spot that many species of fishes, amphibians, and reptiles occupy on the continuum from experimental convenience to ecological importance, as well as on the particular organismal properties that they share, including indeterminate growth and ectothermy. Yet our overall understanding of eco-evolutionary dynamics remains very limited. In the hope of reducing this information gap, the present symposium proceedings include 12 contributions that speak directly to three critical topics in eco-evolutionary dynamics: the role of human influences, constraints and alternatives, and the context dependence of eco-evolutionary dynamics in nature.
Rapid adaptation of defenses can alter ecological dynamics following introduction of a new predator. We tested for local adaptation in Wood Frog (Rana sylvatica) populations that face varying selection from an apex predator, the Marbled Salamander (Ambystoma opacum), which is expanding its distribution in the study region. We performed a reciprocal transplant experiment with Wood Frog eggs and tadpoles and tested survival of tadpoles when exposed to Marbled Salamander larvae in experimental predation trials. We also evaluated life history, behavioral, and morphological trait variation with respect to origin and transplant environments. We found that tadpoles from populations exposed to high risk from Marbled Salamanders survived better when raised in high-risk environments than tadpoles from low-risk populations. However, tadpoles from high-risk environments experienced lower survival than those from low-risk environments when raised in low-risk environments. Development rate, activity, and morphology differed among populations and environments. Faster development of high-risk populations in high-risk environments and activity patterns best explained observed survival differences. These results suggest that tadpoles have evolved adaptive plasticity at microgeographic scales in response to a mosaic of varying predation risk. Fine-scaled evolution of prey survival and local gene flow could enhance the resilience of Wood Frogs to this predator expansion. As warming winters allow Marbled Salamanders to increase in abundance and distribution, the rapid and fine-scaled evolution of their prey could mediate predicted changes to temporary pond communities and ecosystems. Rapid prey evolution might often promote ecological resilience to predator introductions.
Sarah W. Fitzpatrick, Corey A. Handelsman, Julian Torres-Dowdall, Emily W. Ruell, E. Dale Broder, John A. Kronenberger, David N. Reznick, Cameron K. Ghalambor, Lisa M. Angeloni, W. Chris Funk
Theory predicts that gene flow will decrease phenotypic differences among populations. Correlational studies have in some cases documented constraining effects of gene flow on phenotypic divergence and/or have also provided evidence for local differentiation despite high gene flow. However, correlative studies are unable to evaluate how gene flow affects genetically based phenotypic divergence or the extent to which gene flow constrains adaptive divergence. Translocation experiments using Trinidadian guppies provided an opportunity to test the effects of new gene flow on quantitative traits in native recipient populations. We measured a suite of traits in guppies reared in common garden environments before and multiple generations following gene flow from guppies that originated from a different environment. We interpreted our results in light of a priori predictions based on evolutionary theory and extensive background information about guppies and our focal populations. Although we could not include a spatiotemporal control that would allow us to be certain that the observed changes were directly caused by gene flow, we found that post-gene flow populations showed genetically based shifts in most traits. Whether traits shifted in predicted adaptive directions or whether they became more or less similar to the source population depended on the trait and initial conditions of the population. Our study provided a rare opportunity to test how recent gene flow affects genetically based changes in traits with known adaptive significance, and our results attest to the complex interactions between gene flow and selection.
Fishing has caused changes in abundance and demography in exploited populations, in part due to rapid decreases in age and size at maturation. Few models address how direct effects of fishing on age- and size-structure compare to indirect effects on the trophic role of predators. Using Atlantic Cod as example, we model the possible consequences of fishing for trophic roles, contrasting purely demographic effects with those that also include adaptive responses to fishing. While fishing decreases cod abundance in both scenarios, mean trophic level decreases more when there is an adaptive response in maturation. Adaptation also resulted more small fish, which supported the persistence of larger fish, even with heavy fishing. These large fish have a high trophic position, increasing variation relative to the demography-only case. Our model provides a proof-of-concept that eco-evolutionary feedbacks can change the trophic role of fished populations, altering food web dynamics in harvested ecosystems.
Eco-evolutionary dynamics are typically depicted as direct reciprocal interactions between ongoing trait change and ecological change, but environmental context is increasingly recognized for its potential role in mediating evolution's effects on ecology and vice versa. Indeed, environmental context might be considered a third major player within any given eco-evolutionary dynamic, which may at times be determined by strong external drivers but also potentially dynamically remodeled by feedbacks from evolution's effects on ecology. In this study, we test for the environmental context effects of lake trophic state, a condition that is strongly shaped by both external and internal processes of aquatic systems. Specifically, we test whether and how oligotrophic or eutrophic conditions influence the community and ecosystem effects of recent phenotypic divergence of invasive White Perch (Morone americana) populations. Using a factorial treatment design, perch from oligotrophic and eutrophic lake sources were stocked into oligotrophic and eutrophic mesocosms to quantify their effects on pelagic and benthic communities as well as nutrient limitation and system productivity. Perch source influenced benthic invertebrates, primary production, and nutrient limitation, supporting the presence of a phenotype-to-ecology feedback. Importantly, effect size modeling revealed that these perch source effects varied with background trophic conditions and across pelagic versus benthic compartments, supporting context dependence. The specific context-dependent effects we observed suggest that remodeling of environmental context within eco-evolutionary dynamics might facilitate alternate stable state transitions initiated by cultural eutrophication.
Parasites can have important effects on the structure and composition of natural biological communities, either directly by influencing host fecundity and survival (i.e., density-mediated effects) or indirectly by influencing host traits such as behavior, life-history, morphology, and physiology (i.e., trait-mediated effects). Yet few studies have explored how these effects play out in the wild, as opposed to simplified and controlled laboratory or mesocosm settings. We addressed this information gap by translocating Gyrodactylus ectoparasites of the Trinidadian guppy into previously Gyrodactylus-free guppy populations in two rivers (Marianne and Paria) in the Northern Mountain Range in Trinidad. We then measured phenotypic and demographic changes in the guppy host and its competitor, Rivulus hartii, and compared these changes to guppies and Rivulus in control reaches just upstream. In the Marianne, where guppies invest more in reproduction (i.e., greater size and number of embryos), the introduction of Gyrodactylus decreased guppy survival but did not influence guppy density or phenotypes. In the Paria, where guppies invest less in reproduction, the introduction of Gyrodactylus reduced female growth but did not influence guppy survival or density. In neither river did the introduction of Gyrodactylus influence the phenotype or demography of Rivulus. These results indicate some density-mediated and trait-mediated effects of parasites on hosts in natural setting, but also that these effects were context-specific, were generally weak, and did not cascade to a competitor. Give these outcomes, and their difference from typical lab-based studies, it is clear that more studies are needed that experimentally manipulate parasites in natural settings.
Troy N. Simon, Ronald D. Bassar, Andrew J. Binderup, Alex S. Flecker, Mary C. Freeman, James F. Gilliam, Michael C. Marshall, Steven A. Thomas, Joseph Travis, David N. Reznick, Catherine M. Pringle
While previous studies have shown that evolutionary divergence alters ecological processes in small-scale experiments, a major challenge is to assess whether such evolutionary effects are important in natural ecosystems at larger spatial scales. At the landscape scale, across eight streams in the Caroni drainage, we found that the presence of locally adapted populations of guppies (Poecilia reticulata) is associated with reduced algal biomass and increased invertebrate biomass, while the opposite trends were true in streams with experimentally introduced populations of non-locally adapted guppies. Exclusion experiments conducted in two separate reaches of a single stream showed that guppies with locally adapted phenotypes significantly reduced algae with no effect on invertebrates, while non-adapted guppies had no effect on algae but significantly reduced invertebrates. These divergent effects of phenotype on stream ecosystems are comparable in strength to the effects of abiotic factors (e.g., light) known to be important drivers of ecosystem condition. They also corroborate the results of previous experiments conducted in artificial streams. Our results demonstrate that local adaptation can produce phenotypes with significantly different effects in natural ecosystems at a landscape scale, within a tropical watershed, despite high variability in abiotic factors: five of the seven physical and chemical parameters measured across the eight study streams varied by more than one order of magnitude. Our findings suggest that ecosystem structure is, in part, an evolutionary product and not simply an ecological pattern.
An increasingly large number of studies have demonstrated the ability of populations to undergo contemporary or rapid evolution. Little explored in this regard is the role of phenotypic plasticity, although it can influence eco-evolutionary dynamics and hence evolutionary rates. Here we quantify the evolution of life history and plasticity in Trinidadian guppies transplanted from high to novel low predation environments. Common-garden results show that after only nine years, or 13–27 generations, the introduced guppies have diverged from their ancestral population in both litter size and offspring weight and in the plastic response of both traits to food availability. Given these findings, it is clear that local adaptation includes both changes in mean traits and changes in plasticity.
Recent work shows communities and ecosystems can be shaped by predator intraspecific variation, but it is unclear whether the magnitude and direction of these influences are context-dependent. Temperature is an environmental context of strong ecological influence and widespread relevance given global warming trends. Warming should increase per capita predator effects on prey through increases in predator metabolic rate, potentially exacerbating intraspecific differences in ecological effects. Here, we used two populations of the potent pelagic freshwater predator, Western Mosquitofish (Gambusia affinis), to test how experimental pond temperature mediates the differences between their ecological impacts. Mosquitofish introduction induced a strong pelagic trophic cascade, causing a large reduction of crustacean zooplankton biomass, an increase in phytoplankton biomass, and changes to ecosystem-level response variables. Warming ( 2°C above unwarmed treatments) exacerbated fish-induced reduction of zooplankton biomass, but moderated the cascade to phytoplankton, primary productivity, and nutrient concentrations. Effects of intraspecific variation were apparent only on zooplankton, and only at warmed environmental temperatures. The traits underlying this divergence may be related to the population source thermal environments. Overall, results show that warming may increase the ecological importance of predator intraspecific variation. In general, extrinsic environmental drivers, such as those associated with climate change, may reshape the effects of intraspecific trait variation on ecosystems.
The global road network causes many negative ecological effects. Contrasting our knowledge of these effects, insights into evolutionary consequences of roads remain undeveloped. Here, we study a suite of populations of the Wood Frog that appear to be evolving maladaptively in response to road-adjacency. Specifically, when raised together in roadside pools, roadside populations survive at lower rates compared to populations away from roads. To begin to understand the cause of this survival disadvantage, we investigated potential parental and genetic sources of maladaptation. First, to assess whether parental effects might induce maladaptation, we measured adult body weight to length ratio (‘relative weight') and its influence on offspring survival in a reciprocal transplant experiment across 12 populations. Next, to assess whether genetic effects might limit adaptive responses in offspring, we estimated genetic correlations between environments for survival and fitness-related traits. We found that relative weight was higher in roadside populations and, for males, had a positive influence on offspring survival. This demonstrates a novel transgenerational effect of Wood Frog adult males but suggests that this effect is not causing maladaptive survival. Genetic correlations indicated that a subset of roadside genotypes respond adaptively to road-adjacency despite population level maladaptive survival. This suggests that metapopulation dynamics and/or high levels of nonadditive genetic variance may be limiting adaptation or that insufficient time has elapsed for adaptation to occur. Together, these results highlight the complexity and scale of responses to a pervasive feature of landscape alteration revealed by evolutionary approaches.
Only a handful of multi-generational experiments in natural systems of eco-evolutionary dynamics currently exist, despite Fussmann et al.'s call for more such studies nearly a decade ago. To perform such a study, in 2008 we introduced the lizard Leiocephalus carinatus, a predator (and possible food competitor) of the lizard Anolis sagrei, to seven islands having A. sagrei, with seven unmanipulated islands having A. sagrei as controls. Almost immediately, L. carinatus, which is larger and more terrestrial than A. sagrei, caused a major habitat shift in A. sagrei away from the ground and toward higher and thinner perches; focal behavioral surveys showed that on islands where its predator was introduced, A. sagrei had less conspicuous visual displays. The expected pattern for density of A. sagrei is that it would decrease markedly at first via predation from the larger lizard, but then it would increase as the habitat shift selected for individuals better able to live in higher vegetation. Data through 2015 show this pattern, but a return to previous densities (time-by-treatment interaction) was not yet significant. A previous within-generation selection study and comparative data suggest that short legs should evolve as the lizards adapt to better maneuver on the thin perches of higher vegetation. However, no indication of the expected morphological change in limb length was present through 2015. Previous studies showed A. sagrei producing many effects on lower levels of the food web, some quite large. In this study through 2012, we found significant differences only in spiders (web and ground). A possible complication is that the study site was hit by two major hurricanes in the last five years, decreasing population sizes of both lizard species and reducing the experimental perturbations. A benefit of the hurricanes, however, is that they eliminated lizards from some islands, providing the opportunity to monitor natural recolonization, the frequency of which has eco-evolutionary implications. Surveys of the 44 islands that lost lizards showed that recolonization is rather slow. To explore long-term patterns of morphological variation, we monitored morphology of 31 island populations for up to 19 years. Mean limb length oscillated across the 19-year period, both increasing and decreasing substantially, yet the net effect over that period is almost no change. In years following hurricanes, limb length increases significantly more than expected by chance.
There is increasing evidence that closely related species have contrasting ecosystem effects, but very little is known about the temporal scale of these effects. When organisms' ecosystem-effects persist beyond or emerge after their presence in the ecosystem, this might increase the potential for eco-evolutionary feedbacks to accompany evolutionary diversification. Here we studied lab-raised whitefish of a benthic-limnetic species pair from a postglacial adaptive radiation to test whether closely related species have contrasting effects on mesocosm ecosystems (hereafter ecosystem effects). We found that the presence of whitefish (ecological effect) had strong effects on some ecosystem components, for example by reducing snail and mussel abundance and increasing phytoplankton abundance. Whitefish species had contrasting effects (evolutionary effect) on benthic algal cover, dissolved organic carbon, and zooplankton community composition, but these effects only emerged several months after whitefish were removed from the ecosystem. The effects of plasticity and the interactive effects of species and plasticity were relatively weak and, with one exception, not significant. Ecological and evolutionary effect sizes were uncorrelated over both phases of the experiment, as were effect sizes between phases for both ecological and evolutionary contrasts. Overall, our results suggest that adaptive radiation can have effects on the structure and functioning of ecosystems, but that the temporal dynamics and mechanistic basis of these effects are insufficiently understood.
Much of the recent progress in the study of eco-evolutionary dynamics has occurred in fish models. In this review, I focus specifically on the mechanisms by which fish evolution affects ecological processes, highlighting outstanding questions and new frontiers. Fish evolution can alter the ecology of individuals by changing traits that underlie resource use or interactions with other species. Fish eco-evolutionary studies have focused on the ecological consequences of two kinds of effect traits (trophic traits and nutrient recycling traits), but questions remain about the relative influences of genetic and environmental factors. Other fish traits might also have large ecological effects, but we lack frameworks for identifying them, and it remains difficult to link the traits to their ecological consequences. The effect of fish evolution also depends on changes in fish populations, which might vary because of genetic or by environmental factors. Such changes can have dramatic impacts on the expression of effect traits and represent an important, yet largely unexplored conduit linking evolutionary change to community and ecosystem effects. At the level of the community, fish evolution has been shown to induce different kinds of trophic cascades, although it is not clear how patterns observed in simple eco-evolutionary experiments with simple communities are a realistic representation of what happens in complex natural communities. Although fish evolution has also been shown to cause changes in ecosystem function, explaining the mechanisms is difficult because changes in ecosystem function are influenced by changes in all other levels of organization as well as by abiotic heterogeneity. Improving our understanding of the effects of fish evolution on communities and ecosystems will therefore require sophisticated experimental or statistical tools to link causes and effects, and also to complement eco-evolutionary experiments with more studies in natural systems. Continuing to improve our understanding of why fish evolution causes ecological effects will be critical as we expand the scope of studies to include feedbacks, more diverse fish models, and particularly as we apply our understanding of eco-evolutionary dynamics to fish conservation in impacted landscapes.
In 1932, the Tuckasegee Darter was originally described as Poecilichthys gutselli, from the Tuckasegee River (Little Tennessee River system), North Carolina. In 1968, Miller, citing perceived areas of intergradation, relegated it to a subspecies of Etheostoma blennioides. Recent authors, however, re-elevated E. gutselli to the species level without providing any supporting data. We present morphological, meristic, and nuptial male pigmentation data that support the distinctiveness of E. gutselli. Etheostoma gutselli can be distinguished from proximal populations E. blennioides newmanii in the Tennessee River system by lower lateral-line (49–63 vs. 63–81) and caudal-peduncle (18–24 vs. 23–29) scale counts and differences in nuptial male pigmentation. Etheostoma gutselli primarily is restricted to the upper (Blue Ridge) portions of the Little Tennessee and Pigeon river drainages, generally upstream of the Tennessee-North Carolina state line.
Previous work has shown that Centrolene savagei is unique among the more than 150 species in the family Centrolenidae in demonstrating large-male mating advantage. However, it is still unknown whether non-random mating in this species is mediated by intrasexual and/or intersexual selection. To disentangle the effect of these selective pressures on mating pattern in this species, we monitored the breeding behavior of individuals in a population located in the department of Quindío, Central Andes of Colombia. We conducted diurnal and nocturnal surveys each weekend between February and July of 2016 in which we documented morphological (i.e., body size) and behavioral (i.e., chorus tenure, parental-care behavior) characteristics of males to determine their relationship with mating success. We corroborated that in this population of C. savagei, larger males obtain a higher number of mates than do smaller males; male body size co-varies positively with chorus tenure and drives this mating pattern. Male body size was not related to higher fertilization efficiency of eggs laid by females, or a higher survival of embryos in clutches cared for by them. In sum, the higher mating success of larger males in the glassfrog C. savagei seems most strongly related to a mechanism of endurance rivalry competition (intrasexual selection) than female choice (intersexual selection) based on egg fertilization efficiency or parental care quality.
Movement and activity patterns are fundamental to the basic ecology of any organism and can be influenced by a variety of environmental factors. For snakes, which are notable for being secretive and difficult to study, environmental influences on movement are often obscure. Here, we investigate environmental drivers of terrestrial activity for 23 snake species from a temperate community in the Atlantic Coastal Plain region of South Carolina, USA. Activity was strongly seasonal, with primarily fossorial species showing unimodal activity peaks in summer, whereas several aquatic species showed increased terrestrial movements to and from a wetland in both spring and fall. After controlling for seasonal activity, temperature and precipitation had consistent effects on snake movement, with activity of snakes increasing with temperature and decreasing with precipitation. The influence of moon illumination was more ambiguous but may have a weak, negative effect on snake activity. These environmental factors likely drive snake movements because of physiological constraints and trade-offs between foraging success and predation risk. Our results contribute to general knowledge of snake natural history and ecology and may help improve sampling of these elusive organisms that are increasingly in need of conservation attention.
Editor's note.—On 27 July 2017, George Rabb, zoologist and director of the Brookfield Zoo, passed away at the age of 87. He was one of the greatest champions of conservation, and we honor his legacy by reprinting this Historical Perspective that appeared in Copeia (103:1086–1092).
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