Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards

The mechanistic bases of natural and sexual selection on physiological and behavioral traits were examined in male morphs of three colors of the side-blotched lizard, Uta stansburiana. Orange-throated males are aggressive and defend large territories with many females. Blue-throated males defend smaller territories with fewer females; however, blue-throated males assiduously mate guard females on their territory. Yellow-throated males do not defend a territory, but patrol a large home range. They obtain secretive copulations from females on the territories of dominant males. Males with bright orange throats had higher levels of plasma testosterone (T), endurance, activity, and home range size and concomitantly gained greater control over female home ranges than blue- or yellow-throated males. Experimentally elevating plasma T in yellow- and blue-throated males increased their endurance, activity, home range size, and control over female territories to levels that were seen in unmanipulated orange-throated males that had naturally high plasma T. However, the enhanced performance of orange-throated males is not without costs. Orange-throated males had low survival compared to the other morphs. Finally, some yellow-throated males transformed to a partial blue morphology late in the season and the endurance of these transforming yellow-throated males increased from early to late in the season. In addition, yellow-throated males that transformed to blue also had significantly higher plasma T late in the season compared to the plasma T earlier in the season. T appears to play an important role in the physiological changes that all three color morphs undergo during the process of maturation. In some yellow males, T plays an additional role in plastic changes in behavior and physiology late in the reproductive season. We discuss natural and sexual selection on physiological and behavioral traits that leads to the evolution of steroid regulation in the context of alternative male strategies.     

Relatedness,body size and paternity in the alpine newt,Triturus alpestris

Sexual selection has traditionally been investigated assuming that male quality is as skewed as patterns of male reproductive success can sometimes be. Recently, female choice has been investigated under the model of genetic compatibility, which assumes that each individual female has her own 'best' mate and there is no overall optimal choice for all females. We investigated female mate choice in the newt species Triturus alpestris, a member of a genus where female choice has been investigated only within the context of the optimal male (female choice for condition-dependent traits). We provided females with two males that differed in one condition-dependent trait (body size) and overall genetic composition. Both male body size and female body size did not influence paternity, but the degree of genetic relatedness between females and potential mates did. Two components of fitness (fecundity and hatching success) did not differ between singly and multiply sired clutches, indicating that females do not employ polyandry as a means of increasing offspring fitness through genetic bet-hedging. Instead, we hypothesize that females may mate initially for fertility assurance, but prefer less-related males as the most genetically compatible mates.     

Some endocrine traits of transgenic rabbits. I. Changes in plasma and milk hormones

The aim of these studies was to compare some endocrine and non-endocrine characteristics of transgenic (carrying mammary gland-specific mWAP-hFVIII gene construct) and non-transgenic rabbits. The concentrations of corticosterone, progesterone, testosterone, estradiol, insulin-like growth factor I (IGF-I) and human factor VIII (hFVIII) in the blood plasma of adult females (9 months of age, third generation transgenic animals), adult males, and young females (1-2 months of age, fourth generation of transgenic animals), as well as in the milk of lactating adult females, were analyzed by using RIA. In addition, litter size and body mass of pups born by transgenic and non-transgenic females from the third generation were compared. Transgenic animals were compared with their non-transgenic siblings (the same genetic and epigenetic background). Transgenesis did not influence plasma hFVIII, but significantly increased corticosterone (in all animals), reduced IGF-I (in adult males and females), testosterone and estradiol, (in young females) and altered progesterone (increase in adult males and decrease in adult females) concentrations in blood plasma. In addition, transgenic females had higher milk concentrations of testosterone, but not progesterone or IGF-I than their non-transgenic sisters. These endocrine changes were not associated with changes in litter size. Transgenic male (but not female) pups have smaller body mass than control animals. These observations demonstrate the influence of transgenesis per se on the animal growth and endocrine system (secretion of reproductive and stress steroid hormones as well as growth factors) over four generations.     

Phenotypic engineering: using hormones to explore the mechanistic and functional bases of phenotypic variation in nature

Perhaps the best way to determine whether and how traits of organisms are currently adaptive is to alter them experimentally and compare the relative fitness of altered and unaltered individuals. We call this method phenotypic engineering. To the extent that natural selection moulds organisms on a trait-by-trait basis, we would expect fitness of unmanipulated (control) individuals to be higher than that of experimentally altered individuals. However, other outcomes are possible and of interest. If, for example, a single trait were altered and the fitness of manipulated and unmanipulated organisms were found to be similar, we might conclude that selection is not currently operating on the altered trait. Phenotypic engineering with hormones describes an experimental approach to the study of adaptive variation in suites of traits that are hormonally mediated and correlated in their expression. A likely outcome of such manipulations is that some traits would be altered so as to elevate fitness but that changes in other, correlated traits would lower fitness. If the net effect were to depress fitness, a process by which natural selection shapes and maintains organisms as integrated units would be demonstrated. We have employed this approach in studies of the Dark-eyed Junco Junco hyemalis, a small passerine whose reproductive success varies with the abundance of nest predators. We treated males with testosterone, documented the phenotypic consequences and related these to various measures of fitness. Summarizing results to date: Behavioural comparison of males treated with testosterone (T-males) and control males (C-males) shows that T-males sing more frequently, are less attentive to offspring, have larger home ranges and are more attractive to females. Physiologically, testosterone accelerates entry into breeding condition in spring (loss of winter lipid stores) and results in higher levels of corticosterone. If exposure to testosterone is prolonged beyond the breeding season, pre-basic moult is delayed or prevented. We are currently comparing T- and C-males with respect to corticosteroid binding proteins, sperm reserves, response to nestling vocalizations and neuroanatomy. The relationship between testosterone-induced phenotypic variation and fitness is still under study. When treatment extends well beyond the breeding season, testosterone significantly reduces survivorship; otherwise it does not. With respect to apparent reproductive success (i.e. estimates of paternity that are not based on genetic analysis), more young leave the nests of C-males than of T-males, but treatment groups do not differ in the number of young that reach independence. Preliminary data on realized reproductive success (i.e. number of genetic offspring sired) suggest that production as the result of extra-pair fertilizations is greater in T- than in C-males but that T-males lose paternity of more of the offspring of their social mates to other males. Continued investigation will, we hope, reveal the factors governing the trade-offs between male mating effort and parental effort and between survival and current reproduction, as well as the frequency with which the typical phenotype outperforms one that has been experimentally altered.     

Social competition, corticosterone and survival in female lizard morphs

We examined the selective consequences of variation in behaviour and endocrine physiology in two female throat-colour morphs of the lizard, Uta stansburiana in the wild. Female morphs differed in home-range distribution patterns and corticosterone levels in relation to the density and frequency of their female neighbours. Levels of plasma corticosterone of yellow-throated females increased with increased density of both morphs. In contrast, orange-throated females had reduced levels of corticosterone in response to increased density of orange females. Additionally, females with lower corticosterone survived poorly, suggesting that social interactions and high local densities of orange females may be potentially costly for orange females. These results are consistent with decreased fitness effects and suppression of immune function previously reported for orange female morphs surrounded by more orange neighbours. These correlations, in conjunction with previous work in this system, indicate that corticosterone is likely to be an important physiological mechanism regulating female fitness in nature.     

Female freshwater crayfish adjust egg and clutch size in relation to multiple male traits

Females may invest more in reproduction if they acquire mates of high phenotypic quality, because offspring sired by preferred partners may be fitter than offspring sired by non-preferred ones. In this study, we tested the differential maternal allocation hypothesis in the freshwater crayfish, Austropotamobius italicus, by means of a pairing experiment aimed at evaluating the effects of specific male traits (body size, chelae size and chelae asymmetry) on female primary reproductive effort. Our results showed that females laid larger but fewer eggs for relatively small-sized, large-clawed males, and smaller but more numerous eggs for relatively large-sized, small-clawed males. Chelae asymmetry had no effects on female reproductive investment. While the ultimate consequences of this pattern of female allocation remain unclear, females were nevertheless able to adjust their primary reproductive effort in relation to mate characteristics in a species where inter-male competition and sexual coercion may mask or obscure their sexual preferences. In addition, our results suggest that female allocation may differentially affect male characters, thus promoting a trade-off between the expression of different male traits.     

Physiological effects on demography: a long-term experimental study of testosterone's effects on fitness

Understanding physiological and behavioral mechanisms underlying the diversity of observed life-history strategies is challenging because of difficulties in obtaining long-term measures of fitness and in relating fitness to these mechanisms. We evaluated effects of experimentally elevated testosterone on male fitness in a population of dark-eyed juncos studied over nine breeding seasons using a demographic modeling approach. Elevated levels of testosterone decreased survival rates but increased success of producing extra-pair offspring. Higher overall fitness for testosterone-treated males was unexpected and led us to consider indirect effects of testosterone on offspring and females. Nest success was similar for testosterone-treated and control males, but testosterone-treated males produced smaller offspring, and smaller offspring had lower postfledging survival. Older, more experienced females preferred to mate with older males and realized higher reproductive success when they did so. Treatment of young males increased their ability to attract older females yet resulted in poor reproductive performance. The higher fitness of testosterone-treated males in the absence of a comparable natural phenotype suggests that the natural phenotype may be constrained. If this phenotype were to arise, the negative social effects on offspring and mates suggest that these effects might prevent high-testosterone phenotypes from spreading in the population.     

Food, stress, and reproduction: Short-term fasting alters endocrine physiology and reproductive behavior in the zebra finch

Stress is thought to be a potent suppressor of reproduction. However, the vast majority of studies focus on the relationship between chronic stress and reproductive suppression, despite the fact that chronic stress is rare in the wild. We investigated the role of fasting in altering acute stress physiology, reproductive physiology, and reproductive behavior of male zebra finches (Taeniopygia guttata) with several goals in mind. First, we wanted to determine if acute fasting could stimulate an increase in plasma corticosterone and a decrease in corticosteroid binding globulin (CBG) and testosterone. We then investigated whether fasting could alter expression of undirected song and courtship behavior. After subjecting males to fasting periods ranging from 1 to 10 h, we collected plasma to measure corticosterone, CBG, and testosterone. We found that plasma corticosterone was elevated, and testosterone was decreased after 4, 6, and 10 h of fasting periods compared with samples collected from the same males during nonfasted (control) periods. CBG was lower than control levels only after 10 h of fasting. We also found that, coincident with these endocrine changes, males sang less and courted females less vigorously following short-term fasting relative to control conditions. Our data demonstrate that acute fasting resulted in rapid changes in endocrine physiology consistent with hypothalamo-pituitary-adrenal axis activation and hypothalamo-pituitary-gonadal axis deactivation. Fasting also inhibited reproductive behavior. We suggest that zebra finches exhibit physiological and behavioral flexibility that makes them an excellent model system for studying interactions of acute stress and reproduction.     

Behavioral,physiological, and morphological components of dominance and mate attraction in male green iguanas

This study investigated the morphological, physiological, and behavioral components of social dominance important for mate attraction in male green iguanas (Iguana iguana). A group of 9 male and 11 female adult green iguanas was studied in a large semi-natural enclosure during one reproductive season (October–January). Four of the nine males never initiated aggressive encounters; the other five were observed to display aggressively toward each other and were ranked in a linear dominance hierarchy. Head size was the most important factor influencing fighting success. Head size and display frequency were positively correlated with plasma testosterone levels. Dominance rank directly influenced ability to monopolize areas containing resources used by females. The quality of a male's home range, measured as his access to a large basking rock in the enclosure, was related to the proportion of potential mates found within his home range. One male greatly surpassed the others in his ability to defend a home range of high quality and attract potential mates. These data suggest that physiological and morphological factors, through their influence on social behavior, may ultimately affect male reproductive fitness. © 1992 Wiley-Liss, Inc.     

Male mating strategies and the mating system of great-tailed grackles

Great-tailed grackles (Quiscalus mexicanus) are sexually dimorphic,dichromatic, colonially nesting blackbirds. In this study, males pursued three basic types of conditional mating strategies,each of which employed a different set of mating tactics. Territorialmales defended one or more trees in which several females nested.They achieved reproductive success by siring the offspringof their social mates and through extrapair fertilization.Resident males lived in the colony but did not defend territoriesor have social mates. Transient males passed through the colony, staying no more than a few days, and probably visited more thanone colony. Residents appeared to queue for access to territories,but transients did not. Residents and transients gained allpaternity through extrapair fertilizations and provided noparental care. Territorial males sired the majority of offspring,but residents and transients also sired small numbers of nestlings. Territorial males were larger and had longer tails than nonterritorialmales. The number of social mates was related to body size,and males that sired nestlings were heavier and had longertails than males with no genetic reproductive success. Malesthat gained paternity through extrapair fertilization wereheavier and had longer tails than males that did not. The matingsystem of great-tailed grackles can best be categorized as "non-faithful-female frank polygyny."     

Faster lizards sire more offspring: sexual selection on whole-animal performance

Sexual selection operates by acting on variation in mating success. However, since selection acts on whole-organism manifestations (i.e., performance) of underlying morphological traits, tests for phenotypic effects of sexual selection should consider whole-animal performance as a substrate for sexual selection. Previous studies have revealed positive relationships between performance and survival, that is, natural selection, but none have explicitly tested whether performance may influence reproductive success (through more matings), that is, sexual selection. Performance predicts dominance in some species, implying the effects of sexual selection, but how it does so has not been established, nor is it certain whether performance might be a by-product of selection for something else, for example, elevated circulating testosterone levels. We investigated the potential for sexual selection on sprint speed performance in collared lizards (Crotaphytus collaris), considering the potential mediating effects of circulating hormone levels. Among territorial, adult male collared lizards, only sprint speed significantly predicted territory area and number of offspring sired as determined by genetic paternity analysis. Body size, head size, and hind limb length had no effect. Neither plasma testosterone levels nor corticosterone levels correlated with sprint speed, territory area, or number of offspring sired. Thus, our results provide a direct link between whole-animal performance and reproductive success, suggesting that intrasexual selection can act directly on sprint speed performance and drive the evolution of underlying morphological traits.     

Reproductive effort of both male and female Bar‐throated Apalis Apalis thoracica is predicted by ornamentation of self and mate

Melanin‐based plumage ornaments have been shown to play an important role in male–male competition, but also influence inter‐sexual communication. Consequently, ornaments may be associated with reproductive effort of both males and females. Females mated to males with larger melanin ornaments may acquire access to better territories or benefit from increased paternal care. Here we investigated whether the melanin‐based breast‐band of male and female Bar‐throated Apalis Apalis thoracica is a signal of information about its bearer and is associated with male and female reproductive effort. Breast‐band size was a highly variable morphometric trait in both sexes, but only in males was it associated with body mass. We then assessed whether male and female breast‐band size predicted maternal and paternal investment. Egg mass increased with male breast‐band size, but decreased with female breast‐band size. Whether females adjust maternal hormone allocation in response to their partner's ornamentation remains a contentious issue. We found that yolk testosterone and androstenedione concentrations were not predicted by male ornamentation or body mass. Finally, males with larger breast‐bands provided their mates with more food, allowing those females to spend more time incubating. Reproductive effort of both parents is therefore predicted by their own and their mate's ornamentation in Bar‐throated Apalis, and thus breast‐band size potentially acts as a signal of reproductive performance in both sexes. These results highlight the need for more comprehensive analyses of a relationship between melanin‐based ornaments and fitness, incorporating multiple behavioural variables associated with reproductive effort.     

Sex differences in adrenal function in the lizard Cnemidophorus sexlineatus: I. Seasonal variation in the field.

In order to document sex differences in adrenal function and how this relates to gonadal function during the period of seasonal activity, blood samples from male and female six-lined racerunners, Cnemidophorus sexlineatus, were taken immediately after capture in the field for determination of plasma corticosterone and gonadal steroid concentrations. Plasma testosterone and dihydrotestosterone levels for males, and 17 beta-estradiol and progesterone levels for females, were measured. Trends in the concentration of plasma corticosterone differed significantly between males and females. In males the highest concentrations of corticosterone were measured in late spring and the lowest concentrations were measured in late summer. Whereas half of the variation in corticosterone levels among males could be explained as seasonal change, less than 1% of the variation among females could be explained as seasonal change. In males plasma corticosterone and androgens exhibited similar seasonal decreases. Corticosterone levels for females were not correlated with progesterone or 17 beta-estradiol levels. Sex differences in seasonal variation in plasma corticosterone concentrations suggest that corticosterone may be involved in the different reproductive strategies and energy requirements of males and females during the seasonal period of activity.     

Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution?

To explore whether selection for testosterone-mediated traits in males might be constrained by costs of higher testosterone to females, we examined the effects of experimental elevation of plasma testosterone on physiological, reproductive, and behavioral parameters in a female songbird, the dark-eyed junco (Junco hyemalis). We used subcutaneous implants to elevate testosterone (T) in captive and free-living female juncos. In captive birds, we measured the effects of high T on body mass, feather molt, and brood patch formation. In the field, we monitored its effects on the timing of egg laying, clutch size, egg size, egg steroid levels, incubation, and nest-defense behavior. Females implanted with testosterone (T-females) had significantly higher circulating levels of testosterone than did control females (C-females). Captive T-females had lower body mass, were less likely to develop brood patches, and delayed feather molt relative to C-females. Among free-living females, the interval between nest completion and appearance of the first egg was longer for T-females than for C-females and egg yolk concentrations of testosterone were higher, but there were no significant differences in estradiol levels, clutch size, or egg size. Incubation and nest defense behavior were also similar between T- and C-females. Our results suggest that selection on males for higher testosterone might initially lead to a correlated response in females producing changes in body mass and feather molt, both of which could be detrimental. Other possible female responses would be delayed onset of reproduction, which might reduce reproductive success, and higher yolk testosterone, which might have either positive or negative effects on offspring development. We found no reason to expect reduced parental behavior by females as a negative fitness consequence of selection for higher testosterone in males.     

A condition dependent link between testosterone and disease resistance in the house finch.

Testosterone has recently been proposed as a link between male quality and health and the expression of sexual traits. We investigated the relationship between testosterone and measures of the individual condition and health of males in a natural population of house finches (Carpodacus mexicanus). We also conducted a captive experiment in order to test for the effects of testosterone on resistance to coccidia, which is a common parasite of house finches. Free-living males in better condition had higher testosterone levels and lower corticosterone levels than free-living males in poor condition. In our captive experiment, increased testosterone accelerated the rate of coccidial infection as compared with sham-implanted or gonadectomized males. Although the differences were not significant, free-living males infected with coccidia had lower levels of testosterone and higher levels of corticosterone than males that were not infected. Thus, experimentally elevating testosterone levels in captive males resulted in a higher percentage of infected males, while free-living males with coccidial infection had low testosterone levels. This apparent discrepancy between captive and free-living males in the association of testosterone and disease may be explained by the condition dependence of testosterone. These results suggest that the testosterone-dependent sexual traits reliably indicate male overall condition and health and, thus, females could benefit from assessing potential mates based on these traits.     

THE EFFECTS OF THE MATING SYSTEM ON PROGENY PERFORMANCE IN HYLA CRUCIFER (ANURA: HYLIDAE)

We performed a controlled mating experiment to determine whether genetic variation in larval traits in Hyla crucifer was predictable on the basis of mating status or body size of male parent. Larval growth rate was predictably related to body size of the sire. Males from the upper half of the body-size distribution sired offspring with 6% higher growth rates than those of offspring sired by males from the lower half of the body-size distribution. Offspring sired by males that obtained mates in nature had 3% higher growth rates than their half-siblings sired by males that did not mate in nature. Genetic variation for larval-period duration and size at metamorphosis was detected; however, neither mating status nor body size of sire could be used to predict values of these traits in the progeny. Although all three larval traits can affect fitness, there was no evidence that the offspring of some sires would always outperform the offspring of others in all three traits. The predictable association between adult male size and larval growth rate means that the H. crucifer mating system would have a directional effect on larval growth rate if male body size influences the outcome of male-male competition or female choice.     

Does catch and release affect the mating system and individual reproductive success of wild Atlantic salmon (Salmo salar L.)?

In this study, we documented the breeding system of a wild population of Atlantic salmon (Salmo salar L.) by genetically sampling every returning adult and assessed the determinants of individual fitness. We then quantified the impacts of catch and release (C&R) on mating and reproductive success. Both sexes showed high variance in individual reproductive success, and the estimated standardized variance was higher for males (2.86) than for females (0.73). We found a weak positive relationship between body size and fitness and observed that fitness was positively correlated with the number of mates, especially in males. Mature male parr sired 44% of the analysed offspring. The impact of C&R on the number of offspring was size dependent, as the reproductive success of larger fish was more impaired than smaller ones. Also, there was an interactive negative effect of water temperature and air exposure time on reproductive success of C&R salmon. This study improves our understanding of the complex reproductive biology of the Atlantic salmon and is the first to investigate the impact of C&R on reproductive success. Our study expands the management toolbox of appropriate C&R practices that promote conservation of salmon populations and limit negative impacts on mating and reproductive success.     

Home ranges in adult Scandinavian brown bears (Ursus arctos): effect of mass, sex, reproductive category, population density and habitat type

Annual home-range size indices for 36 male and 52 female adult brown bears Ursus arctos in two study areas in central and northern Scandinavia were estimated to evaluate factors believed to influence home-range size. Male home ranges were larger than home ranges of lone females after controlling for the sexual size dimorphism acting on metabolic needs. Further, home ranges of females with cubs were smaller than home ranges of lone females and females with yearlings. Thus, differences in metabolic need were not able to explain the variation in range size among females of different reproductive categories or between males and females, suggesting roaming behaviour of males in this promiscuous species. Home-range size in both males and females was inversely related to population density along a density gradient that was not linked to food availability. This contradicts the hypothesis that females use the minimum areas that sustain their energy requirements. However, on a large geographical scale a negative relationship between range size and food availability was evident. The annual home ranges in inland boreal environments in Scandinavia are the largest reported for brown bears in Eurasia, and similar to those in inland boreal and montane environments in North America.     

Males' evolutionary responses to experimental removal of sexual selection

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.