Evolutionary Dynamics of Rapid, Microgeographic Adaptation in an Amphibian Metapopulation

Wild organisms can rapidly adapt to changing environments, even at fine spatial scales. This fact prompts hope that contemporary local adaptation may buffer some of the negative anthropogenic impacts to ecosystems. However, there are limits to the pace of adaptation. Understanding the adaptive potential—and limitations—of individual species at fine-resolution is an important task if we hope to accurately predict the repercussions of future climate and landscape change on biodiversity. My dissertation takes advantage of an uncommonly long-observed and closely-studied system to paint a comprehensive picture of evolution over time in association with shifts in ecological contexts. In this dissertation, I show evidence of rapid, microgeographic evolution in response to climate within a metapopulation of wood frogs (Rana sylvatica). Critically, I show that populations separated by tens to hundreds of meters—well within the dispersal ability of the species—exhibited considerable shifts in development rates over a period of two decades, or roughly 6-9 generations. Using historical climate data and new methods of assessing landscape change, I show that these changes were mainly a response to warming climates. The ecological contexts experienced by the metapopulation are associated with the evolution of physiological rates. Specifically, I show that climate change seems to have caused a counter-intuitive delay in spring breeding phenology while drought and warming later in the larval development period correspond with a shift toward earlier metamorphosis. The picture that emerges is of a contracting developmental window, which is expected to select for faster intrinsic development rates. Superimposed on the metapopulation-wide shift to faster development was a pattern of counter-gradient variation reflecting a similar pattern seen two decades prior. Furthermore, I empirically demonstrate a trade-off between faster development and a swimming performance trait that strongly contributes to fitness. This trade-off helps to explain why intrinsic development rates vary spatially with pond temperatures, but in the opposite direction of the relationship with temperature over time. Though the evidence for rapid adaptation to climate change presented in this dissertation reveals that evolution can buffer populations from extinction, it also entreats caution. There is a clear trend of demographic decline among wood frog populations that experienced greater magnitudes of environmental change. In fact, the three populations that suffered local extinctions over the 20-year course of observations inhabited ponds characterized by the greatest change in temperature or canopy

Anti-oxidative cellular protection effect of fasting-induced autophagy as a mechanism for hormesis

The aim of this investigation was to test the hypothesis that fasting-induced augmented lysosomal autophagic turnover of cellular proteins and organelles will reduce potentially harmful lipofuscin (age-pigment) formation in cells by more effectively removing oxidatively damaged proteins. An animal model (marine snail - common periwinkle, Littorina littorea) was used to experimentally test this hypothesis. Snails were deprived of algal food for 7 days to induce an augmented autophagic response in their hepatopancreatic digestive cells (hepatocyte analogues). This treatment resulted in a 25% reduction in the cellular content of lipofuscin in the digestive cells of the fasting animals in comparison with snails fed ad libitum on green alga (Ulva lactuca). Similar findings have previously been observed in the digestive cells of marine mussels subjected to copper-induced oxidative stress. Additional measurements showed that fasting significantly increased cellular health based on lysosomal membrane stability, and reduced lipid peroxidation and lysosomal/cellular triglyceride. These findings support the hypothesis that fasting-induced augmented autophagic turnover of cellular proteins has an anti-oxidative cytoprotective effect by more effectively removing damaged proteins, resulting in a reduction in the formation of potentially harmful proteinaceous aggregates such as lipofuscin. The inference from this study is that autophagy is important in mediating hormesis. An increase was demonstrated in physiological complexity with fasting, using graph theory in a directed cell physiology network (digraph) model to integrate the various biomarkers. This was commensurate with increased health status, and supportive of the hormesis hypothesis. The potential role of enhanced autophagic lysosomal removal of damaged proteins in the evolutionary acquisition of stress tolerance in intertidal molluscs is discussed and parallels are drawn with the growing evidence for the involvement of autophagy in hormesis and anti-ageing processes

FUNCTIONAL MORPHOLOGY AND PERFORMANCE OF ECOLOGICAL SYSTEMS WITH EXTREME PRESSURES: WATERFALL CLIMBING AND PREDATOR-PREY INTERACTION IN AMPHIDROMOUS GOBIOID FISHES

Understanding the functional capacity and performance of organisms provides a strong foundation for recognizing the forces that are responsible for their form, and how they might adapt to variable or changing environmental conditions. Amphidromous stream goby fishes live in a habitat subject to two potentially extreme selective pressures: (1) predation on juvenile fish returning to freshwater from the ocean, and (2) the demand to climb waterfalls to reach adult breeding habitats. Recognizing these selection pressures, I present studies evaluating (1) the mechanisms underlying the functional capacity for adhesive performance, and (2) the risk that predation imposes on amphidromous gobies. Specifically, these evaluations are based on measurements of the musculoskeletal biomechanics underlying adhesive performance in climbing and non-climbing species of gobies, and measurements of feeding kinematics and performance by piscivorous gobioid predators attacking juvenile gobies. Through the biomechanical and functional studies I present, we reach better understandings of how the functional demands of an extreme habitat are met across a range of related species

Ecosystem Impacts of Consumer Evolution: Intraspecific Variation in the Elemental Phenotype of Aquatic Consumers

abstract: Primary production in aquatic ecosystems is often limited by the availability of nitrogen (N) and/or phosphorus (P). Animals can substantially alter the relative availability of these nutrients by storing and recycling them in differential ratios. Variation in these stoichiometric traits, i.e., the elemental phenotype, within a species can link organismal evolution to ecosystem function. I examined the drivers of intraspecific variation in the elemental phenotype of aquatic consumers to test for the generality of these effects. Over a thermal gradient in Panamá, I found that average specific growth grate and body P content of the mayfly Thraulodes increased with environmental temperature, but that these patterns were due to site-specific differences rather than the direct effects of warmer temperature. In a meta-analysis of published studies, I found that in fishes intraspecific variation in dietary N:P ratio had a significant effect on excretion N:P ratio, but only when accounting for consumption. I tested for the effects of variation in consumption on excretion N:P ratio among populations of the fish Gambusia marshi in the Cuatro Ciénegas basin in Coahuila, Mexico. G. marshi inhabits warm groundwater-fed springs where it often co-occurs with predatory fishes and cool runoff-dominated wetlands which lack predators. Using stoichiometric models, I generated predictions for how variation in environmental temperature and predation pressure would affect the N:P ratio recycled by fishes. Adult female G. marshi excretion N:P ratio was higher in runoff-dominated sites, which was consistent with predators driving increased consumption rates by G. marshi. This result was supported by a diet ration manipulation experiment in which G. marshi raised on an ad libitum diet excreted N:P at a lower ratio than fish raised on a restricted diet ration. To further support the impacts of predation on phenotypic diversification in G. marshi, I examined how body morphology varied among habitats and among closely related species. Both among and within species, predation had stronger effects on morphology than the physical environment. Overall, these results suggest that predation, not temperature, has strong effects on these phenotypic traits of aquatic consumers which can alter their role in ecosystem nutrient cycling through variation in consumption rates.Dissertation/ThesisDoctoral Dissertation Biology 201

Developmental origin underlies evolutionary rate variation across the placental skull

The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull's major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation. This article is part of the theme issue 'The mammalian skull: development, structure and function'

Developmental origin underlies evolutionary rate variation across the placental skull

The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull's major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation. This article is part of the theme issue 'The mammalian skull: development, structure and function'