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Although behavior may often be a fairly direct target of natural or sexual selection, it cannot evolve without changes in subordinate traits that cause or permit its expression. In principle, changes in endocrine function could be a common mechanism underlying behavioral evolution because they are well positioned to mediate integrated responses to behavioral selection. More specifically, hormones can influence both motivational (e.g., brain) and performance (e.g., muscles) components of behavior simultaneously and in a coordinated fashion. If the endocrine system is often “used” as a general mechanism to effect responses to selection, then correlated responses in other aspects of behavior, life history, and organismal performance (e.g., locomotor abilities) should commonly occur because any cell with appropriate receptors could be affected. Ways in which behavior coadapts with other aspects of the phenotype can be studied directly through artificial selection and experimental evolution. Several studies have targeted rodent behavior for selective breeding and reported changes in other aspects of behavior, life history, and lower-level effectors of these organismal traits, including endocrine function. One example involves selection for high levels of voluntary wheel running, one aspect of physical activity, in four replicate High Runner (HR) lines of mice. Circulating levels of several hormones (including insulin, testosterone, thyroxine, triiodothyronine) have been characterized, three of which—corticosterone, leptin, and adiponectin—differ between HR and control lines, depending on sex, age, and generation. Potential changes in circulating levels of other behaviorally and metabolically relevant hormones, as well as in other components of the endocrine system (e.g., receptors), have yet to be examined. Overall, results to date identify promising avenues for further studies on the endocrine basis of activity levels.

The insulin and insulin-like signaling (IIS) molecular network regulates cellular growth and division, and influences organismal metabolism, growth and development, reproduction, and lifespan. As a group, reptiles have incredible diversity in the complex life history traits that have been associated with the IIS network, yet the research on the IIS network in ectothermic reptiles is sparse. Here, we review the IIS network and synthesize what is known about the function and evolution of the IIS network in ectothermic reptiles. The primary hormones of this network—the insulin-like growth factors 1 and 2 (IGFs) likely function in reproduction in ectothermic reptiles, but the precise mechanisms are unclear, and likely range from influencing mating and ovulation to maternal investment in embryonic development. In general, plasma levels of IGF1 increase with food intake in ectothermic reptiles, but the magnitude of the response to food varies across species or populations and the ages of animals. Long-term temperature treatments as well as thermal stress can alter expression of genes within the IIS network. Although relatively little work has been done on IGF2 in ectothermic reptiles, IGF2 is consistently expressed at higher levels than IGF1 in juvenile ectothermic reptiles. Furthermore, in contrast to mammals that have genetic imprinting that silences the maternal IGF2 allele, in reptiles IGF2 is bi-allelically expressed (based on findings in chickens, a snake, and a lizard). Evolutionary analyses indicate some members of the IIS network are rapidly evolving across reptile species, including IGF1, insulin (INS), and their receptors. In particular, IGF1 displays extensive nucleotide variation across lizards and snakes, which suggests that its functional role may vary across this group. In addition, genetic variation across families and populations in the response of the IIS network to environmental conditions illustrates that components of this network may be evolving in natural populations. The diversity in reproductive physiology, metabolic plasticity, and lifespan among reptiles makes the study of the IIS network in this group a potentially rich avenue for insight into the evolution and function of this network. The field would benefit from future studies that discern the respective functions of IGF1 and IGF2 and how these functions vary across taxa, perfecting additional assays for measuring IIS components, and determining the role of IIS in different tissues.

The endocrine mechanisms causing variation and plasticity in life history traits (e.g., development time, mass at birth/hatching, rate of postnatal growth, age or size at sexual maturity, litter or clutch size, annual survival, and lifespan) or fitness (annual or lifetime reproductive success) have recently garnered considerable interest. We review three issues facing studies that quantify relationships between endocrine traits and life histories or measures of fitness and describe possible solutions using insights from evolutionary ecology. We focus in particular on the steroid hormones glucocorticoids that are involved in the vertebrate neuroendocrine stress response. First, context-dependent associations between endocrine traits and life histories or fitness are widespread, and therefore, it is important to quantify how intrinsic or extrinsic factors modify these relationships. Second, studies in evolutionary endocrinology may aspire to quantify patterns of natural selection on endocrine traits, but this may not tell us how they influence fitness. Studies that also identify the actual targets of selection that the endocrine traits are influencing will be very useful. Third, environmental or intrinsic factors can cause co-variance between endocrine traits and life histories or fitness. This is problematic for interpreting the potential evolutionary consequences of selection on endocrine traits, but it can also produce divergent answers for relationships between endocrine traits and life histories or fitness depending upon whether the data are analyzed in an among- or within-year framework. Future long-term studies following uniquely marked individuals over their lifetime (longitudinal individual-based approach) in combination with experimental manipulations of the endocrine traits or environmental factors influencing both endocrine traits and life histories or fitness may help to produce new insights in evolutionary endocrinology despite these issues. This is an ambitious endeavor, and we briefly review some of the key issues facing such long-term studies and experimental manipulations of endocrine traits.

Evolutionary endocrinology represents a synthesis between comparative endocrinology and evolutionary genetics. This synthesis can be viewed through the breeder’s equation, a cornerstone of quantitative genetics that, in its univariate form, states that a population’s evolutionary response is the product of the heritability of a trait and selection on that trait (R = h²S). Under this framework, evolutionary endocrinologists have begun to quantify the heritability of, and the strength of selection on, a variety of hormonal phenotypes. With specific reference to our work on testosterone and corticosterone in birds and lizards, we review these studies while emphasizing the challenges of applying this framework to hormonal phenotypes that are inherently plastic and mediate adaptive responses to environmental variation. Next, we consider the untapped potential of evolutionary endocrinology as a framework for exploring multivariate versions of the breeder’s equation, with emphasis on the role of hormones in structuring phenotypic and genetic correlations. As an extension of the familiar concepts of phenotypic integration and hormonal pleiotropy, we illustrate how the hormonal milieu of an individual acts as a local environment for the expression of genes and phenotypes, thereby influencing the quantitative genetic architecture of multivariate phenotypes. We emphasize that hormones are more than mechanistic links in the translation of genotype to phenotype: by virtue of their pleiotropic effects on gene expression, hormones structure the underlying genetic variances and covariances that determine a population’s evolutionary response to selection.

Synopsis All organisms must anticipate and balance energetic demands and available resources in order to maximize fitness. As hormones coordinate many interactions between an organism’s internal condition and the external environment, they may be key in mediating the allocation of resources to meet these demands. However, given that individuals differ considerably in how they react to changes in energetic demand, we asked whether variations in endocrine traits also correspond with life history variation. We tested whether natural variation in glucocorticoid hormone levels, oxidative stress measurements, and condition related to reproductive effort in a free-living songbird, the tree swallow, Tachycineta bicolor. We then tested whether any of these traits predicted the probability of a particular individual’s return to the local population in the following two years, an indicator of survival in this philopatric species. We found that males and females with longer telomeres had lighter nestlings. Moreover, individuals with lower plasma antioxidant capacity and higher reactive oxygen metabolites (i.e., greater oxidative stress) were less likely to return to the population. However, none of these traits were related to glucocorticoid levels. Our findings suggest a trade-off between reproduction and survival, with individuals with shorter telomeres having heavier nestlings but potentially paying a cost in terms of higher oxidative stress and lower survival. Interestingly, the evidence of this trade-off was unrelated to natural variation in glucocorticoids.

Hormones are dynamic signaling molecules that influence gene activity and phenotype, and they are thus thought to play a central role in phenotypic evolution. In vertebrates, many fitness-related traits are mediated by the hormone testosterone (T), but the mechanisms by which T levels evolve are unclear. Here, we summarize a series of studies that advance our understanding of these mechanisms by comparing males from two subspecies of dark-eyed junco (Junco hyemalis) that differ in aggression, body size, and ornamentation. We first review our research demonstrating population differences in the time-course of T production, as well as findings that point to the gonad as a major source of this variation. In a common garden, the subspecies do not differ in pituitary output of luteinizing hormone, but males from the more androgenized subspecies have greater gonadal gene expression for specific steroidogenic enzymes, and they may be less sensitive to feedback along the hypothalamo-pituitary-gonadal (HPG) axis. Furthermore, we present new data from a common garden study demonstrating that the populations do not differ in gonadal sensitivity to gonadotropin-inhibitory hormone (i.e., GnIH receptor mRNA abundance), but the more androgenized subspecies expresses less gonadal mRNA for glucocorticoid receptor and mineralocorticoid receptor, suggesting altered cross-talk between the hypothalamo-pituitary-gonadal and -adrenal axes as another mechanism by which these subspecies have diverged in T production. These findings highlight the diversity of mechanisms that may generate functional variation in T and influence hormone-mediated phenotypic evolution.

The network of the interactions among genes, proteins, and metabolites delineates a range of potential phenotypic diversifications in a lineage, and realized phenotypic changes are the result of differences in the dynamics of the expression of the elements and interactions in this deterministic network. Regulatory mechanisms, such as hormones, mediate the relationship between the structural and dynamic properties of networks by determining how and when the elements are expressed and form a functional unit or state. Changes in regulatory mechanisms lead to variable expression of functional states of a network within and among generations. Functional properties of network elements, and the magnitude and direction of evolutionary change they determine, depend on their location within a network. Here, we examine the relationship between network structure and the dynamic mechanisms that regulate flux through a metabolic network. We review the mechanisms that control metabolic flux in enzymatic reactions and examine structural properties of the network locations that are targets of flux control. We aim to establish a predictive framework to test the contributions of structural and dynamic properties of deterministic networks to evolutionary diversifications.

It is well understood that much of evolutionary change is mediated through the endocrine system with growing interest to identify how this occurs. This however, causes a conflict of sorts. To understand endocrine mechanism, a focus on detail is required. In contrast, to understand evolutionary change, reduction to a few key traits is essential. Endocrine proxies, measurable traits that accurately reflect specific hormonal titers or the timing of specific hormonal events, can reduce endocrine complexity to a few traits that enable predictions of how the endocrine system regulates evolutionary change. In the tobacco hornworm (Manduca sexta, Sphingidae), three endocrine proxies, measured on 5470 individuals, were used to test explicit predictions of how the endocrine system regulates the response to 10 generations of simultaneous selection on body size and development time. The critical weight (CW) reflects the variation in the cessation of juvenile hormone (JH) secretion in the last larval instar, the interval to cessation of growth (ICG) reflects the variation in prothoracicotropic hormone and 20-hydroxyecdysone (20E). Growth rate (GR) reflects the nutrient signaling pathways, primarily the insulin and TOR This is a standard identity similar to DNA signaling pathways. These three endocrine proxies explained 99% and 93% of the variation in body size and development time, respectively, following the 10 generations of simultaneous selection. When the two focal traits, body size and development time, were selected in the same direction, both to either increase or both to decrease, the response to selection was determined primarily by the CW and the ICG, proxies for the developmental hormones JH and 20E, and constrained by GR. In contrast, when the two focal traits were selected in opposite directions, one to increase and the other to decrease, the response to selection was determined primarily by the insulin and TOR signaling pathways as measured by their proxy, GR, and constrained by the CW and the ICG. Thus, the use of endocrine proxies may be a powerful tool to reduce endocrine complexity to enable explicit and testable predictions how the endocrine system can enable or constrain evolutionary change.

Daily rhythms for hormonal traits are likely widespread and important aspects of organismal (e.g., life history) adaptation. Yet they remain substantially understudied, especially with respect to variable rhythms within species. The cricket, Gryllus firmus, exhibits a genetically polymorphic circadian rhythm for the blood titer of the key hormone, juvenile hormone (JH). Gryllus firmus is also wing-polymorphic, consisting of a dispersing morph that delays reproduction and a flightless morph with substantially enhanced egg production. JH circadian phenotype strongly covaries with morph type: The blood JH titer is strongly rhythmic in multiple populations artificially-selected for the dispersing morph (LW(f)=long wings with functional flight muscles) and is essentially arrhythmic in populations selected for the SW (short-winged) morph. Association between JH titer cycle and LW(f) morph is also found in natural populations of G. firmus and in several related species in the field. This is one of the very few studies of endocrine titer variation in natural populations of an insect. The morph-specific cycle is underlain by a circadian rhythm in hormone biosynthesis, which in turn is underlain by a rhythm in a brain neuropeptide regulator of JH biosynthesis. The morph-specific JH titer circadian cycle is also strongly correlated with a morph-specific daily rhythm in global gene expression. This is currently the only example of a genetically-variable hormone circadian rhythm in both the laboratory and field that is strongly associated with an ecologically important polymorphism. The extensive information on the underlying causes of the morph-specific JH titer rhythm, coupled with the strong association between the JH circadian rhythm and wing polymorphism makes this system in G. firmus an exceptional experimental model to investigate the mechanisms underlying circadian hormonal adaptations. Genetic polymorphism for the JH titer circadian rhythm in G. firmus is discussed in context of circadian rhythms for endocrine traits reported for vertebrates and insects. Consequences of the failure to identify endocrine circadian rhythms on the accuracy of estimation of quantitative-genetic parameters, such as heritability and correlations between hormonal and fitness-related traits, are also discussed.