Nutritional constraints on brain evolution: Sodium and nitrogen limit brain size.

Nutrition has been hypothesized as an important constraint on brain evolution. However, it is unclear whether the availability of specific nutrients or the difficulty of locating high-quality diets limits brain evolution, especially over long periods of time. We found that dietary nutrient content predicted brain size across 42 species of butterflies. Brain size, relative to body size, was associated with the sodium and nitrogen content of a species' diet. There was no evidence that host plant apparency (measured by plant height) was related to brain evolution. The timing of diet shifts across species varied from 3.5 to 90 million years ago, but nutritional constraints did not lessen over time as species adapted to a diet. Although nutrition was linked to overall brain volume, there was no evidence that nutrition was related to the relative size of individual brain regions. Laboratory rearing experiments confirmed the underlying assumption of most comparative studies that the majority of interspecific trait variation stems from genetically based differences across species rather than developmental plasticity. This study highlights a novel role of sodium and nitrogen in brain evolution, which is additionally interesting given current anthropogenic change in the availability of these nutrients.

Does Hormonal Pleiotropy Shape the Evolution of Performance and Life History Traits?

SYNOPSIS: Hormonal pleiotropy occurs when a part of the endocrine system (e.g., hormone concentrations) influences the expression of two or more phenotypes. Although hormonal pleiotropy may have similar evolutionary consequences as genetic pleiotropy, most conceptual and empirical work on its putative evolutionary consequences to date has focused on identifying whether the different components of an endocrine axis (titer, receptor expression, etc.) that affect trait expression are themselves able to evolve independently from one another. This is important because if these different components evolve together, the expression of two traits affected by the same hormone may be yoked and evolve non-independently. Here, we first describe methodological approaches used to identify how hormonal pleiotropy could cause the co-evolution of performance and life history traits. We then focus on a similar but less studied concept about how hormonal pleiotropy can affect phenotypic responses to selection. If the expression of two traits is affected by the same hormone, the magnitude of the phenotypic response to selection may be exacerbated or retarded compared to the absence of this hormonal pleiotropy. We use classical concepts from quantitative genetics to discuss an approach for identifying whether hormonal pleiotropy has such evolutionary consequences using data collected from longitudinal studies of wild animals. We develop a simple quantitative genetics model to derive predictions about the conditions under which hormonal pleiotropy would affect the response to selection. We focus on performance and life history traits and how the effects of hormonal pleiotropy on the evolution of these traits depend upon the genetic correlations between the hormone and traits as well as the direction and strength of selection on the two traits. Finally, we review the literature for examples that have estimated these model parameters to characterize the studies that have or have not found support for these model predictions.

Nutrition shapes life-history evolution across species.

Nutrition is a key component of life-history theory, yet we know little about how diet quality shapes life-history evolution across species. Here, we test whether quantitative measures of nutrition are linked to life-history evolution across 96 species of butterflies representing over 50 independent diet shifts. We find that butterflies feeding on high nitrogen host plants as larvae are more fecund, but their eggs are smaller relative to their body size. Nitrogen and sodium content of host plants are also both positively related to eye size. Some of these relationships show pronounced lineage-specific effects. Testis size is not related to nutrition. Additionally, the evolutionary timing of diet shifts is not important, suggesting that nutrition affects life histories regardless of the length of time a species has been adapting to its diet. Our results suggest that, at least for some lineages, species with higher nutrient diets can invest in a range of fitness-related traits like fecundity and eye size while allocating less to each egg as offspring have access to a richer diet. These results have important implications for the evolution of life histories in the face of anthropogenic changes in nutrient availability.

Cryptic individual scaling relationships and the evolution of morphological scaling.

Morphological scaling relationships between organ and body size-also known as allometries-describe the shape of a species, and the evolution of such scaling relationships is central to the generation of morphological diversity. Despite extensive modeling and empirical tests, however, the modes of selection that generate changes in scaling remain largely unknown. Here, we mathematically model the evolution of the group-level scaling as an emergent property of individual-level variation in the developmental mechanisms that regulate trait and body size. We show that these mechanisms generate a "cryptic individual scaling relationship" unique to each genotype in a population, which determines body and trait size expressed by each individual, depending on developmental nutrition. We find that populations may have identical population-level allometries but very different underlying patterns of cryptic individual scaling relationships. Consequently, two populations with apparently the same morphological scaling relationship may respond very differently to the same form of selection. By focusing on the developmental mechanisms that regulate trait size and the patterns of cryptic individual scaling relationships they produce, our approach reveals the forms of selection that should be most effective in altering morphological scaling, and directs researcher attention on the actual, hitherto overlooked, targets of selection.

Brain size predicts problem-solving ability in mammalian carnivores.

Despite considerable interest in the forces shaping the relationship between brain size and cognitive abilities, it remains controversial whether larger-brained animals are, indeed, better problem-solvers. Recently, several comparative studies have revealed correlations between brain size and traits thought to require advanced cognitive abilities, such as innovation, behavioral flexibility, invasion success, and self-control. However, the general assumption that animals with larger brains have superior cognitive abilities has been heavily criticized, primarily because of the lack of experimental support for it. Here, we designed an experiment to inquire whether specific neuroanatomical or socioecological measures predict success at solving a novel technical problem among species in the mammalian order Carnivora. We presented puzzle boxes, baited with food and scaled to accommodate body size, to members of 39 carnivore species from nine families housed in multiple North American zoos. We found that species with larger brains relative to their body mass were more successful at opening the boxes. In a subset of species, we also used virtual brain endocasts to measure volumes of four gross brain regions and show that some of these regions improve model prediction of success at opening the boxes when included with total brain size and body mass. Socioecological variables, including measures of social complexity and manual dexterity, failed to predict success at opening the boxes. Our results, thus, fail to support the social brain hypothesis but provide important empirical support for the relationship between relative brain size and the ability to solve this novel technical problem.

A molecular signaling approach to linking intraspecific variation and macro-evolutionary patterns.

Macro-evolutionary comparisons are a valued tool in evolutionary biology. Nevertheless, our understanding of how systems involved in molecular signaling change in concert with phenotypic diversification has lagged. We argue that integrating our understanding of the evolution of molecular signaling systems with phylogenetic comparative methods is an important step toward understanding the processes linking variation among individuals with variation among species. Focusing mostly on the endocrine system, we discuss how the complexity and mechanistic nature of molecular signaling systems may influence the application and interpretation of macro-evolutionary comparisons. We also detail five hypotheses concerning the role that physiological mechanisms can play in shaping macro-evolutionary patterns, and discuss ways in which these hypotheses could influence phenotypic diversification. Finally, we review a series of tools able to analyze the complexity of physiological systems and the way they change in concert with the phenotypes for which they coordinate development.

Insulin-like growth factor-1 is associated with life-history variation across Mammalia.

Despite the diversity of mammalian life histories, persistent patterns of covariation have been identified, such as the 'fast-slow' axis of life-history covariation. Smaller species generally exhibit 'faster' life histories, developing and reproducing rapidly, but dying young. Hormonal mechanisms with pleiotropic effects may mediate such broad patterns of life-history variation. Insulin-like growth factor 1 (IGF-1) is one such mechanism because heightened IGF-1 activity is related to traits associated with faster life histories, such as increased growth and reproduction, but decreased lifespan. Using comparative methods, we show that among 41 mammalian species, increased plasma IGF-1 concentrations are associated with fast life histories and altricial reproductive patterns. Interspecific path analyses show that the effects of IGF-1 on these broad patterns of life-history variation are through its direct effects on some individual life-history traits (adult body size, growth rate, basal metabolic rate) and through its indirect effects on the remaining life-history traits. Our results suggest that the role of IGF-1 as a mechanism mediating life-history variation is conserved over the evolutionary time period defining mammalian diversification, that hormone-trait linkages can evolve as a unit, and that suites of life-history traits could be adjusted in response to selection through changes in plasma IGF-1.

Developmental constraints on behavioural flexibility.

We suggest that variation in mammalian behavioural flexibility not accounted for by current socioecological models may be explained in part by developmental constraints. From our own work, we provide examples of constraints affecting variation in behavioural flexibility, not only among individuals, but also among species and higher taxonomic units. We first implicate organizational maternal effects of androgens in shaping individual differences in aggressive behaviour emitted by female spotted hyaenas throughout the lifespan. We then compare carnivores and primates with respect to their locomotor and craniofacial adaptations. We inquire whether antagonistic selection pressures on the skull might impose differential functional constraints on evolvability of skulls and brains in these two orders, thus ultimately affecting behavioural flexibility in each group. We suggest that, even when carnivores and primates would theoretically benefit from the same adaptations with respect to behavioural flexibility, carnivores may nevertheless exhibit less behavioural flexibility than primates because of constraints imposed by past adaptations in the morphology of the limbs and skull. Phylogenetic analysis consistent with this idea suggests greater evolutionary lability in relative brain size within families of primates than carnivores. Thus, consideration of developmental constraints may help elucidate variation in mammalian behavioural flexibility.

Multiple determinants of whole and regional brain volume among terrestrial carnivorans.

Mammalian brain volumes vary considerably, even after controlling for body size. Although several hypotheses have been proposed to explain this variation, most research in mammals on the evolution of encephalization has focused on primates, leaving the generality of these explanations uncertain. Furthermore, much research still addresses only one hypothesis at a time, despite the demonstrated importance of considering multiple factors simultaneously. We used phylogenetic comparative methods to investigate simultaneously the importance of several factors previously hypothesized to be important in neural evolution among mammalian carnivores, including social complexity, forelimb use, home range size, diet, life history, phylogeny, and recent evolutionary changes in body size. We also tested hypotheses suggesting roles for these variables in determining the relative volume of four brain regions measured using computed tomography. Our data suggest that, in contrast to brain size in primates, carnivoran brain size may lag behind body size over evolutionary time. Moreover, carnivore species that primarily consume vertebrates have the largest brains. Although we found no support for a role of social complexity in overall encephalization, relative cerebrum volume correlated positively with sociality. Finally, our results support negative relationships among different brain regions after accounting for overall endocranial volume, suggesting that increased size of one brain regions is often accompanied by reduced size in other regions rather than overall brain expansion.

Mediation of vertebrate life histories via insulin-like growth factor-1.

Life-history traits describe parameters associated with growth, size, survival, and reproduction. Life-history variation is a hallmark of biological diversity, yet researchers commonly observe that one of the major axes of life-history variation after controlling for body size involves trade-offs among growth, reproduction, and longevity. This persistent pattern of covariation among these specific traits has engendered a search for shared mechanisms that could constrain or facilitate production of variation in life-history strategies. Endocrine traits are one candidate mechanism that may underlie the integration of life history and other phenotypic traits. However, the vast majority of this research has been on the effects of steroid hormones such as glucocorticoids and androgens on life-history trade-offs. Here we propose an expansion of the focus on glucocorticoids and gonadal hormones and review the potential role of insulin-like growth factor-1 (IGF-1) in shaping the adaptive integration of multiple life-history traits. IGF-1 is a polypeptide metabolic hormone largely produced by the liver. We summarize a vast array of research demonstrating that IGF-1 levels are susceptible to environmental variation and that IGF-1 can have potent stimulatory effects on somatic growth and reproduction but decrease lifespan. We review the few studies in natural populations that have measured plasma IGF-1 concentrations and its associations with life-history traits or other characteristics of the organism or its environment. We focus on two case studies that found support for the hypothesis that IGF-1 mediates adaptive divergence in suites of life-history traits in response to varying ecological conditions or artificial selection. We also examine what we view as potentially fruitful avenues of research on this topic, which until now has been rarely investigated by evolutionary ecologists. We discuss how IGF-1 may facilitate adaptive plasticity in life-history strategies in response to early environmental conditions and also how selection on loci controlling IGF-1 signaling may mediate population divergence and eventual speciation. After consideration of the interactions among androgens, glucocorticoids, and IGF-1 we suggest that IGF-1 be considered a suitable candidate mechanism for mediating life-history traits. Finally, we discuss what we can learn about IGF-1 from studies in free-ranging animals. The voluminous literature in laboratory and domesticated animals documenting relationships among IGF-1, growth, reproduction, and lifespan demonstrates the potential for a number of new research questions to be asked in free-ranging animals. Examining how IGF-1 mediates life-history traits in free-ranging animals could lead to great insight into the mechanisms that influence life-history variation.

Lifetime selection on a hypoallometric size trait in the spotted hyena.

Size-related traits are common targets of natural selection, yet there is a relative paucity of data on selection among mammals, particularly from studies measuring lifetime reproductive success (LRS). We present the first phenotypic selection analysis using LRS on size-related traits in a large terrestrial carnivore, the spotted hyena, which displays a rare pattern of female-biased sexual size dimorphism (SSD). Using path analysis, we investigate the operation of selection to address hypotheses proposed to explain SSD in spotted hyenas. Ideal size measures are elusive, and allometric variation often obfuscates interpretation of size proxies. We adopt a novel approach integrating two common methods of assessing size, and demonstrate lifetime selection on size-related traits that scale hypoallometrically with overall body size. Our data support selection on hypoallometric traits in hyenas, but not on traits exhibiting isometric or hyperallometric scaling relationships, or on commonly used measures of overall body size. Our results represent the first estimate of lifetime selection on a large carnivore, and suggest a possible route for maintenance of female-biased SSD in spotted hyenas. Finally, our results highlight the importance of choosing appropriate measures when estimating animal body size, and suggest caution in interpreting selection on size-related traits as selection on size itself.