Ellen D. Ketterson

Hormones and Life Histories: An Integrative Approach

This article, which focuses on hormones and the diverse effects they have on behavior and physiology, raises evolutionary questions that hormonal studies appear especially well suited to address. These include the endocrine basis for life-history trade-offs, the role of hormones in adaptive alterations in social organization and mating systems, and whether natural selection acts on traits or organisms. The article also shows how phenotypic engineering by hormonal manipulations can reveal the evolutionary significance of phenotypic variation. By generating rare or novel phenotypes, we can attempt to determine the shape of fitness profiles in nature. To illustrate phenotypic engineering, we manipulated plasma testosterone in a freeliving bird, the dark-eyed junco (Junco hyemalis), and measured the effects of the treatment on behavior, including allocation of time to mate attraction and parental behavior as well as use of space, and on physiology, including regulation of body mass, corticosterone, and molt. We compared treated males to controls for various correlates of fitness, including territory acquisition, mate acquisition, mate retention, physical condition of the mate, apparent reproductive success, extrapair fertilizations, and survival. The results to date appear to indicate that selection is relatively indifferent to a broad range of phenotypes, while extreme deviations from the norm are selected against.

ADAPTATION, EXAPTATION, AND CONSTRAINT : A HORMONAL PERSPECTIVE

We approach conceptual issues in evolutionary biology from an endocrinological perspective, noting that single hormones typically act on several target tissues and thereby mediate suites of correlated phenotypic traits. When several components of such a suite are beneficial, an important evolutionary question is whether all are adaptations or some are exaptations. The answer may depend on whether the traits arose in response to selection on variation in systemic levels of the hormone on variation in responsiveness of target tissues to invariant levels of the hormone. If the former, selection probably acted directly on fewer than all traits; beneficial traits arising indirectly would be exaptations. In contrast, multiple beneficial traits that arose out of independent changes in target‐tissue sensitivity to invariant hormone levels could all be adaptations. Knowledge of specific hormonal mechanisms as well as of historical selective regimes will be necessary to draw such distinctions. Endocrine constraints on evolution can be studied experimentally by applying hormones systemically and measuring interdependent responses of beneficial and detrimental traits to selection (phenotypic engineering with hormones). Supposing that alteration of one trait in isolation would enhance fitness, cases in which the net effect of endocrine alteration of multiple traits is to depress fitness provide evidence for constraints. We briefly report results of recent studies employing hormonal manipulations, stressing our own work on the dark‐eyed junco (Junco hyemalis: Emberizidae).

TESTOSTERONE AND AVIAN LIFE HISTORIES: EFFECTS OF EXPERIMENTALLY ELEVATED TESTOSTERONE ON BEHAVIOR AND CORRELATES OF FITNESS IN THE DARK-EYED JUNCO (JUNCO HYEMALIS)

Hormones influence many aspects of organismal behavior, physiology, and morphology, and thus hormones may lie at the root of many life-history trade-offs. By manipulating hormones we can create novel phenotypes (i.e., perform phenotypic engineering) and attempt to relate phenotypic variation to fitness. We report the effect of testosterone treatment on parental behavior and vocal behavior of adult male dark-eyed juncos. Testosterone partially suppressed paternal behavior and increased the frequency of song. When we compared treated males and controls for nine potential correlates of fitness (offspring growth and survival to the age of 10 d, condition of females, length of the interval between consecutive nestings, size of subsequent clutches and broods, mate retention within and between breeding seasons, and survival rate), we found no statistical differences. In some measures treated males outperformed controls, but in most the reverse was true. The power of some of our tests was not great enough to detect small differences. At this stage of our investigation, three interpretations of our results seem almost equally probable: (1) a broad range of behavioral phenotypes is selectively neutral in the junco, (2) male parental behavior is beneficial to males only in some years or habitats, or (3) we have yet to measure the correlates of fitness that are most strongly affected by the behavioral changes induced by elevated testosterone.

Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission

The past 30 years of immunological research have revealed much about the proximate mechanisms of maternal antibody transmission and utilization, but have not adequately addressed how these issues are related to evolutionary and ecological theory. Much remains to be learned about individual differences within a species in maternal antibody transmission as well as differences among species in transmission or utilization of antibodies. Similarly, maternal-effects theory has generally neglected the mechanisms by which mothers influence offspring phenotype. Although the environmental cues that generate maternal effects and the consequent effects for offspring phenotype are often well characterized, the intermediary physiological and developmental steps through which the maternal effect is transmitted are generally unknown. Integration of the proximate mechanisms of maternal antibody transmission with evolutionary theory on maternal effects affords an important opportunity to unite mechanism and process by focusing on the links between genetics, environment and physiology, with the ultimate goal of explaining differences among individuals and species in the transfer of immune function from one generation to the next.

Geographic Variation and Its Climatic Correlates in the Sex Ratio of Eastern‐Wintering Dark‐Eyed Juncos (Junco Hyemalis Hyemalis)

The sex ratio of Dark-eyed Juncos wintering in the eastern and central United States and Canada varies clinally along a latitudinal gradient. The percentage of Y Y among both museum skins and live-caught birds is 70% in the south, 20% in the north. When abundance according to latitude is also considered, an average Y appears to winter farther south than an average 8 and hence probably tends to migrate farther. Latitude alone is an excellent predictor of sex ratio (r2 = 85%), and latitude plus 13 other measures of climate explain virtually all the variation (r2 - 96.6%). Extreme measures of climate, as compared to mean measures, are equally predictive. Principal component analysis indicates that snowfall, temperature, and latitude are the most important climatic variables associated with sex ratio. Because 8 8 average larger than Y y and are concentrated northward, mean wing length increases with latitude and is significantly correlated with climatic measures that vary with latitude. Further, larger birds within each sex may select higher altitudes as wintering sites. Sex ratio does not vary measurably with date in wintering populations. Among possible explanations for clinal variation in sex ratio are sex-associated differences in (1) advantages of early arrival on the breeding or -wintering grounds, (2) impacts of inter- and intrasexual competition, and (3) effects of low temperature and intermittent food avail- ability. Comparison of ; ; and Y Y with respect to potential fasting endurance, a size-related metabolic parameter, indicates that at OC an average 8 should be able to fast 4% longer (1.6 h) than an average Y at standard metabolic rates. An extremely heavy 8 might endure fasting up to 29% (10.7 h) longer than a very light Y. These differences may confer greater survival ability upon the 8 at latitudes where snow cover can often preclude feeding.

The Evolution of Differential Bird Migration

The evolution of bird migration and the role of migration in life history have long been matters of general interest, and the volume of recent literature on these subjects (Baker, 1978; Dingle, 1980; Gauthreaux, 1978, 1979, 1982; Fretwell, 1980; Greenberg, 1980; Greenwood, 1980; Myers, 1981a; Ketterson and Nolan, 1982) reflects their continuing importance to students of avian ecology and evolutionary biology.

Testosterone in Females: Mediator of Adaptive Traits, Constraint on Sexual Dimorphism, or Both?

When selection on males and females differs, the sexes may diverge in phenotype. Hormones serve as a proximate regulator of sex differences by mediating sex‐biased trait expression. To integrate these perspectives, we consider how suites of traits mediated by the same hormone in both sexes might respond to selection. In male birds, plasma testosterone (T) varies seasonally and among species according to mating system. When elevated experimentally, it is known to enhance some components of fitness and to decrease others. We report that female T also varies seasonally and co‐varies with male T. Female T is higher in relation to male T in sexually monomorphic species and is higher absolutely in females of species with socially monogamous mating systems, which suggests adaptation. We also consider the effect of experimentally elevated T on females and whether traits are sensitive to altered T. We hypothesize that sensitive traits could become subject to selection after a natural change in T and that traits with opposing fitness consequences in males and females could constrain dimorphism. Results from birds, including the dark‐eyed junco (Junco hyemalis), reveal many sensitive traits, some of which appear costly and may help to account for observed levels of sexual dimorphism.

Steroid Hormones and Immune Function: Experimental Studies in Wild and Captive Dark‐Eyed Juncos (Junco hyemalis)

Monogamous and polygynous male songbirds generally differ in their breeding season profiles of circulating testosterone. Testosterone level spikes early in the breeding season of monogamists and then declines, but it remains high in polygynists. Male dark‐eyed juncos (Junco hyemalis) are socially monogamous and exhibit the usual pattern, but experimental maintenance of high testosterone throughout the breeding season alters normal behavior and physiology and affects various components of annual reproductive success but not overall annual success. Because stabilizing selection predicts that alteration of naturally existing phenotypes should reduce lifetime reproductive success, we asked whether prolonged testosterone exposure might impair immune function and perhaps thereby reduce life span. We assessed immune function in captive and wild male juncos that we treated with either testosterone‐filled or empty Silastic implants. Results indicate that prolonged elevation of testosterone suppresses antibody production in captive males and cell‐mediated immunity in wild males. Together these results suggest that testosterone‐treated males may be more susceptible to disease or parasitic infection. As earlier studies have shown, levels of corticosterone as well as testosterone are higher in testosterone‐treated males, so it is unclear whether the immune suppression we observed is due to testosterone’s direct effects on immunity or testosterone’s influence on glucocorticoid production. We discuss results in the context of recent hypotheses regarding life‐history theory and potential endocrine‐immune interactions.

Testosterone and avian life histories: the effect of experimentally elevated testosterone on corticosterone and body mass in dark-eyed juncos.

To assess whether alterations in the normal pattern of testosterone (T) secretion might be beneficial or detrimental, we studied a breeding population of dark-eyed juncos in which we elevated T experimentally and measured its effect on potential correlates of fitness. We treated both free-living and captive males with implants that were either empty (C-males, controls) or packed with T (T-males, experimentals). Timing of implant varied and was designed to mimic natural peak breeding levels except that peaks were either prolonged or premature. We bled the birds at recapture and analyzed their plasma, and that of their female mates, for T and corticosterone (B). We also measured body mass and fat score in free-living T- and C-males. In the field, T-implants elevated T and kept it elevated for at least a month. Experimental males also had higher B than controls. In captives, the effect of the implants on plasma T was detectable within 24 hr. B in captive T-males was again higher than in captive C-males. In females, neither T nor B differed between mates of T- and C-males. T-males implanted in early spring lost more mass between implant and recapture in late spring than did controls and also had lower fat scores when recaptured. When implants were inserted in summer, treatment did not influence mass. Elevated T in early spring apparently hastened the transition from the winter to the breeding mode of fat storage. We suggest that prolonged elevation of testosterone might be selected against because of the association between T and B. Premature elevation of T might be costly because of the resultant loss of mass and fat reserves, which could lead to mortality when spring snowstorms prevent access to food.

Natural Variation in a Testosterone‐Mediated Trade‐Off between Mating Effort and Parental Effort

Male birds frequently face a trade‐off between acquiring mates and caring for offspring. Hormone manipulation studies indicate that testosterone often mediates this trade‐off, increasing mating effort while decreasing parental effort. Little is known, however, about individual covariation between testosterone and relevant behavior on which selection might act. Using wild, male dark‐eyed juncos (Junco hyemalis), we measured individual variation in testosterone levels before and after standardized injections of gonadotropin‐releasing hormone (GnRH). The GnRH challenges have been shown to produce short‐term testosterone increases that are similar to those produced naturally in response to social stimuli, repeatable in magnitude, and greater in males with more attractive ornaments. We correlated these testosterone increases with behavioral measures of mating and parental effort (aggressive response to a simulated territorial intrusion and nestling feeding, respectively). Males that showed higher postchallenge testosterone displayed more territorial behavior, and males that produced higher testosterone increases above initial levels displayed reduced parental behavior. Initial testosterone levels were positively but nonsignificantly correlated with aggression but did not predict parental behavior. These relationships suggest that natural variation in testosterone, specifically the production of short‐term increases, may underlie individual variation in the mating effort/parental effort trade‐off. We discuss the implications of these results for the evolution of hormonally mediated trade‐offs.