Selection on dispersal drives evolution of metabolic capacities for energy production in female wing-polymorphic sand field crickets, Gryllus firmus

Life history and metabolism covary, but the mechanisms and individual traits responsible for these linkages remain unresolved. Dispersal capability is a critical component of life histories that is constrained by metabolic capacities for energy production. Conflicting relationships between metabolism and life histories may be explained by accounting for variation in dispersal and maximal metabolic rates. We used female wing-polymorphic sand field crickets, Gryllus firmus, selected either for long wings (LW) and flight-capability or short wings (SW) and high early lifetime fecundity to test the hypothesis that selection on dispersal capability drives the evolution of metabolic capacities. While resting metabolic rates were similar, long-winged crickets reached higher maximal metabolic rates than short-winged crickets, resulting in improved running performance. We further provided insight into the mechanisms responsible for covariation between life history and metabolism by comparing mitochondrial content of tissues involved in powering locomotion and assessing function of mitochondria isolated from long- and short-winged crickets. This demonstrated that larger metabolic capacities in long-winged crickets were underpinned by increases in mitochondrial content of dorsoventral flight muscle and enhanced bioenergetic capacities of mitochondria within the fat body, a tissue responsible for fuel storage and mobilization. Thus, selection on flight-capability remodels metabolism in a trait and tissue-specific manner to enlarge metabolic capacities necessary for dispersal

Mechanistic basis of life history strategies: Behavioral and metabolic plasticity supports flight or reproduction in wing-polymorphic field crickets

Energy available for life history allocations or investments into growth, reproduction, activity, and somatic maintenance depends on how much and what type of resources organisms acquire from the environment, combined with how acquired resources are processed through metabolic pathways. Consequently, both environmental (e.g. resource availability) and physiological (e.g. metabolic) constraints on energy availability directly contribute to the maintenance of widescale variation in life histories across the tree of life. Variation in life history spans a single continuum from a fast (fast growth, early reproduction, and short lifespan) to slow (slow growth, late reproduction, and long lifespan) “pace-of-life” that shapes population and ecosystem dynamics. The timing of life history allocations evolves to maximize fitness based on environmental conditions, but environments are becoming more variable, due to global climate change. Organisms may be able to adapt to novel environments by changing their life history but, predicting if and how life history evolution will buffer species from consequences of global change requires a mechanistic understanding of life history, motivating this dissertation work. Decades of work has investigated the roles of energetic constraints in shaping life history allocations, but environmental constraints on resource acquisition and physiological constraints on metabolism are often considered independent of one another. Therefore, complex interactions between resource acquisition, metabolism, and life history allocations, along with their role in governing life history evolution, remains uncharacterized in any single system. This dissertation sheds new light on the mechanistic underpinnings of life history by testing the central hypothesis that to meet changing energetic demands of life history allocations through the life cycle, coordinated shifts in resource acquisition and metabolism are required, and therefore underpin the expression of alternative life histories. While large-scale diversity in life histories is found across the tree of life, variation in life history strategies is also present among individuals in species with life history polymorphisms. I leveraged one model system with a life history polymorphism, wing-polymorphic field crickets (Gryllus spp.). Within populations of wing-polymorphic field cricket species, individuals are either flight-capable (long-winged, LW) or flightless (short-winged, SW) in early adulthood. The polymorphism is maintained by an allocation-based trade-off between flight and oogenesis: long-winged crickets preferentially allocate resources to support flight muscle maintenance and somatic fat storage, enhancing dispersal capability, while short-winged crickets preferentially allocate resources to support oogenesis at a younger age, enhancing early life fecundity. Both long- and short-winged forms (morphs) co-occur within populations and the polymorphism is present in multiple independently evolving lineages of field crickets. Thus, this system provides a powerful model in which we can investigate mechanisms of life history evolution acting on genetically similar organisms, both within and across species. I studied two closely related wing-polymorphic cricket species, the variable field cricket (Gryllus lineaticeps) (Chapter 1 and 3) and the sand field cricket (Gryllus firmus) (Chapter 2 and 3). The variable field crickets (G. lineaticeps) that I worked with were derived from wild-collected individuals and maintained in a genetically polymorphic laboratory population, providing morphs with a mixed genetic background and naturally segregating combinations of alleles that evolved under natural selection. In complement, the sand field crickets (G. firmus) that I worked with were derived from family lines following long-term artificial selection on wing-length, which maximized phenotypic and genetic differences between flight-capable and flightless crickets. In these species, I advanced our understanding of the behavioral and physiological basis of life history, by characterizing the associations between resource acquisition, metabolism, and life history allocations in crickets investing in either flight or reproduction. To do so, I applied an integrative approach that spanned levels of the biological hierarchy (whole organism, tissues, cells, and organelles) on variable timescales (within and across life stages). Combined, my findings suggest that both resource acquisition and metabolism are fine-tuned based on energetic demands of life history, and thus represent fundamental processes that have evolved to enable organisms to alter the timing of major life history events.In Chapter 1, I disentangled the reciprocal interaction between resource acquisition and life history allocations, by using a geometric framework of nutrition experimental approach. I hypothesized that high demands of biosynthesis for life history allocations drive elevated resource acquisition requirements and increase performance costs of resource limitations. To test this hypothesis, I characterized resource acquisition (dietary preferences and intake) and life history allocations, across the juvenile to adulthood transition in both male and female variable field crickets (Gryllus lineaticeps), when feeding on artificial diets varying in nutrient composition (carbohydrate- or protein-biased). I used Gryllus lineaticeps crickets recently derived from natural populations for this study, to avoid potential effects of long-term lab adaptation on nutritional preferences and feeding behavior. Consistent with my hypothesis, long-winged crickets increase feeding as juveniles to meet elevated caloric requirements associated with flight muscle synthesis. However, nutritionally imbalanced diets did not affect allocations to flight because long-winged juveniles behaviorally adjusted feeding to meet caloric requirements irrespective of diet composition and palatability. As adults, males ate less than females and life history allocations of males were insensitive to diet, due to lower energetic costs of reproduction for males compared to females in early adulthood. In females, the onset of adulthood was accompanied by a shift in dietary preferences to more protein-biased diets in short-winged crickets investing in large scale and rapid oogenesis, but not in long-winged crickets investing in flight. Unlike juveniles, adult females did not fully behaviorally compensate for variation in diet composition and incurred large caloric and protein deficits on a carbohydrate-biased diet. This in turn resulted in a constraint on reproductive investment by short-winged females; on carbohydrate-biased diets, short-winged females could no longer meet biosynthetic demands of oogenesis, resulting in small ovaries. This finding broadly suggests that when energetic and nutrient demands of life history allocations are large, behavioral adjustments in feeding may not be sufficient to buffer organisms from energetic constraints caused by resource limitations. Additionally, on a carbohydrate-biased diet, ovary size of short-winged and long-winged crickets was similar suggesting that without sufficient protein acquisition, the adaptive benefit of higher early life fecundity associated with the typical short-winged life history strategy is lost. Together these findings reveal that strong associations between resource acquisition and life history allocations dictate fitness consequences of reductions in environmental resource availabilities in a life stage, sex, and life history specific manner. In Chapter 2, I focused on the association between metabolic and life history evolution. In the sand field cricket, Gryllus firmus, I determined how high energetic demands of life history allocations to dispersal-capability drives the evolution of larger metabolic capacities through biochemical and molecular changes in tissues and organelles. I hypothesized that tissue-specific increases in either mitochondrial content or function result in larger metabolic capacities and improved locomotor performance in flight-capable long-winged compared to flightless short-winged crickets, due to the high aerobic demands of flight. I measured a suite of metabolic traits across levels of the biological hierarchy, from organismal metabolic rates and running performance in vivo, to metabolic function of tissues and organelles in vitro. When running on a treadmill, flight-capable long-winged crickets reach higher maximal metabolic rates and had an enhanced endurance compared to flightless short-winged crickets. Consistent with my hypothesis, long-winged crickets also exhibited increases in mitochondrial content of dorsoventral flight muscle and modifications to the electron transport system composition within mitochondria of the fat body, a tissue responsible for fuel storage and mobilization, which resulted in enhanced mitochondrial bioenergetic capacities. Therefore, metabolic pathways are remodeled in a tissue-specific manner to increase energy production capacities required for high levels of activity. Since this study was conducted in sand field crickets (Gryllus firmus) artificially selected for flight-capability or reproduction, I further concluded that differences in metabolic capacities arose in response to selection on a single life history trait, dispersal-capability. Overall, this work provides fresh insight into the links between life history and metabolism, suggesting that dispersal capability should be explicitly considered as a potential factor driving the evolution of metabolic capacities.In Chapter 3, I further investigated the interaction between metabolism and life history by determining if mitochondrial function and life history allocations change concurrently across early adulthood. I hypothesized that energetic requirements increase with biosynthetic demands of life history and elicit concurrent elevations in mitochondrial respiratory function. To test this hypothesis, I assessed life history allocations and mitochondrial function across the first week of adulthood, in both long- and short-winged variable field (Gryllus lineaticeps) and sand field (Gryllus firmus) crickets. In both species, mitochondrial function of morphs diverged through time, along with their allocations to either flight or reproduction. In long-winged crickets, mitochondrial bioenergetic capacity for energy production increases through early adulthood, peaks at the time of dispersal, but rapidly declines when a switch to reproduction is made post-dispersal. In short-winged crickets, mitochondrial bioenergetic capacity declines gradually as ovarian synthesis is completed. Despite different evolutionary histories (Gryullus firmus- artificially selected vs. Gryllus lineaticeps- genetically admixed backgrounds), patterns of mitochondrial plasticity were consistent between species, suggesting that mitochondrial plasticity is likely an important general adaptation shaped by life history evolution. Overall, these findings support the conclusion that adaptive plasticity in mitochondrial function enables shifts in life history allocations, advancing our understanding of the metabolic basis of life history

Socioecological Variables Predict Telomere Length in Wild Spotted Hyenas

Telomeres are regarded as important biomarkers of ageing and serve as useful tools in revealing how stress acts at the cellular level. However, the effects of social and ecological factors on telomere length remain poorly understood, particularly in free-ranging mammals. Here, we investigated the influences of within-group dominance rank and group membership on telomere length in wild adult spotted hyenas (Crocuta crocuta). We found large effects of both factors; high-ranking hyenas exhibited significantly greater mean telomere length than did subordinate animals, and group membership significantly predicted mean telomere length within high-ranking females. We further inquired whether prey availability mediates the observed effect of group membership on telomere length, but this hypothesis was not supported. Interestingly, adult telomere length was not predicted by age. Our work shows for the first time, to the best of our knowledge, the effects of social rank on telomere length in a wild mammal and enhances our understanding of how social and ecological variables may contribute to organismal senescence

Selection on dispersal drives evolution of metabolic capacities for energy production in female wing-polymorphic sand field crickets, Gryllus firmus.

Life history and metabolism covary, but the mechanisms and individual traits responsible for these linkages remain unresolved. Dispersal capability is a critical component of life history that is constrained by metabolic capacities for energy production. Conflicting relationships between metabolism and life histories may be explained by accounting for variation in dispersal and maximal metabolic rates. We used female wing-polymorphic sand field crickets, Gryllus firmus, selected either for long wings (LW, flight-capable) or short wings (SW, flightless) to test the hypothesis that selection on dispersal capability drives the evolution of metabolic capacities. While resting metabolic rates were similar, long-winged crickets reached higher maximal metabolic rates than short-winged crickets, resulting in improved running performance. We further provided insight into the mechanisms responsible for covariation between life history and metabolism by comparing mitochondrial content of tissues involved in powering locomotion and assessing the function of mitochondria isolated from long- and short-winged crickets. Our results demonstrated that larger metabolic capacities in long-winged crickets were underpinned by increases in mitochondrial content of dorsoventral flight muscle and enhanced bioenergetic capacities of mitochondria within the fat body, a tissue responsible for fuel storage and mobilization. Thus, selection on flight capability correlates with increases in maximal, but not resting metabolic rates, through modifications of tissues powering locomotion at the cellular and organelle levels. This allows organisms to meet high energetic demands of activity for life history. Dispersal capability should therefore explicitly be considered as a potential factor driving the evolution of metabolic capacities

Data from: Voluntary locomotor activity mitigates oxidative damage associated with isolation stress in the prairie vole (Microtus ochrogaster)

Organismal performance directly depends on an individual's ability to cope with a wide array of physiological challenges. For social animals, social isolation is a stressor that has been shown to increase oxidative stress. Another physiological challenge, routine locomotor activity, has been found to decrease oxidative stress levels. Because we currently do not have a good understanding of how diverse physiological systems like stress and locomotion interact to affect oxidative balance, we studied this interaction in the prairie vole (Microtus ochrogaster). Voles were either pair housed or isolated and within the isolation group, voles either had access to a moving wheel or a stationary wheel. We found that chronic periodic isolation caused increased levels of oxidative stress. However, within the vole group that was able to run voluntarily, longer durations of locomotor activity were associated with less oxidative stress. Our work suggests that individuals who demonstrate increased locomotor activity may be better able to cope with the social stressor of isolation

Voluntary locomotor activity mitigates oxidative damage associated with isolation stress in the prairie vole (Microtus ochrogaster)

Organismal performance directly depends on an individual's ability to cope with a wide array of physiological challenges. For social animals, social isolation is a stressor that has been shown to increase oxidative stress. Another physiological challenge, routine locomotor activity, has been found to decrease oxidative stress levels. Because we currently do not have a good understanding of how diverse physiological systems like stress and locomotion interact to affect oxidative balance, we studied this interaction in the prairie vole (Microtus ochrogaster). Voles were either pair housed or isolated and within the isolation group, voles either had access to a moving wheel or a stationary wheel. We found that chronic periodic isolation caused increased levels of oxidative stress. However, within the vole group that was able to run voluntarily, longer durations of locomotor activity were associated with less oxidative stress. Our work suggests that individuals who demonstrate increased locomotor activity may be better able to cope with the social stressor of isolation

Voluntary locomotor activity mitigates oxidative damage associated with isolation stress in the prairie vole (Microtus ochrogaster)

Organismal performance directly depends on an individual's ability to cope with a wide array of physiological challenges. For social animals, social isolation is a stressor that has been shown to increase oxidative stress. Another physiological challenge, routine locomotor activity, has been found to decrease oxidative stress levels. Because we currently do not have a good understanding of how diverse physiological systems like stress and locomotion interact to affect oxidative balance, we studied this interaction in the prairie vole (Microtus ochrogaster). Voles were either pair housed or isolated and within the isolation group, voles either had access to a moving wheel or a stationary wheel. We found that chronic periodic isolation caused increased levels of oxidative stress. However, within the vole group that was able to run voluntarily, longer durations of locomotor activity were associated with less oxidative stress. Our work suggests that individuals who demonstrate increased locomotor activity may be better able to cope with the social stressor of isolation

Voluntary locomotor activity mitigates oxidative damage associated with isolation stress in the prairie vole ( Microtus ochrogaster

Organismal performance directly depends on an individual's ability to cope with a wide array of physiological challenges. For social animals, social isolation is a stressor that has been shown to increase oxidative stress. Another physiological challenge, routine locomotor activity, has been found to decrease oxidative stress levels. Because we currently do not have a good understanding of how diverse physiological systems like stress and locomotion interact to affect oxidative balance, we studied this interaction in the prairie vole (Microtus ochrogaster). Voles were either pair housed or isolated and within the isolation group, voles either had access to a moving wheel or a stationary wheel. We found that chronic periodic isolation caused increased levels of oxidative stress. However, within the vole group that was able to run voluntarily, longer durations of locomotor activity were associated with less oxidative stress. Our work suggests that individuals who demonstrate increased locomotor activity may be better able to cope with the social stressor of isolation

Vole exercise oxidative stress data

This file includes all data for the study (vole IDs, exercise distance, and oxidative stress markers)