Variability of GnRH secretion in two goby species with socially controlled alternative male mating tactics

Male reproductive phenotypic plasticity related to environmental-social conditions is common among teleost fish. In several species, males adopt different mating tactics depending on their size, monopolizing mates when larger, while parasitizing dominant male spawns when smaller. Males performing alternative mating tactics are often characterized by a strong dimorphism in both primary and secondary reproductive traits. According to studies on sex-changing species and on species where only one male morph is reproductively active, male alternative phenotypes are expected to vary also in gonadotropin-releasing hormone (GnRH) neurons in forebrain preoptic area (POA). Here, we compared the intra- and inter-sexual variations in number and size of GnRH neurons, along with gonads and male accessory structure investment, in two goby species, the grass goby, Zosterisessor ophiocephalus, and the black goby, Gobius niger, characterized by male alternative mating phenotypes. In both species, older and larger males defend nests, court and perform parental care, while younger and smaller ones try to sneak territorial male spawning. We found that grass goby and black goby have different patterns of GnRH expression. Grass goby presents a clear intra-sexual dimorphism in GnRH expression, related to the occurrence of alternative mating tactics, while in the black goby, only inter-sexual differences are observed. The inter- and intra-specific variability in the GnRH neurons in these two goby species is discussed in light of the differences in migratory behavior, nest type, and mating system.     

Correlation between Male Social Status,Testosterone Levels,and Parasitism in a Dimorphic Polygynous Mammal

Life history trade-offs have often been assumed to be the consequence of restrictions in the availability of critical resources such as energy and nutrients, which necessitate the differential allocation of resources to costly traits. Here, we examined endocrine (testosterone) and health (parasite burdens) parameters in territorial and non-territorial New Zealand fur seal males. We documented intra-sexual differences in sexual behaviours, testosterone levels, and parasitism that suggest a trade-off exists between reproductive success and physical health, particularly susceptibility to helminths and acanthocephalans, in males displaying different mating tactics (i.e., territorial and non-territorial tactics). Levels of testosterone were higher in territorial males and correlated positively with reproductive effort (i.e., intra- and inter-sexual interactions). However, these territorial males also exhibited high levels of parasitic infection, which may impair survival in the long-term. Our study, while limited in sample size, provides preliminary evidence for a link between male mating tactics, testosterone levels and parasite loads, and potential effects on reproductive success and life history that should be explored further.     

Endocrine and behavioral changes in male African elephants: linking hormone changes to sexual state and reproductive tactics

Hormones play a crucial role in mediating genetic and environmental effects into morphological and behavioral phenotypes. In systems with alternative reproductive tactics (ART) shifts between tactics are hypothesized to be under proximate hormonal control. Most studies of the underlying endocrine changes behind ART have focused on fish and amphibians rather than mammals and few have investigated the potential interaction between different endocrine axes in regulating shifts between conditional dependent tactics. Using a combination of endocrine and behavioral data from male African elephants we expand on our previously published analysis and show that the initial increase in androgens predates the behavioral shifts associated with reproductively active periods, supporting the role of androgens in activating sexually active periods in males. A strong interactive effect between androgens and glucocorticoids was found to determine the presence or absence of temporal gland secretion and urine dribbling, signals associated with the competitive reproductive tactic of musth, with elevated glucocorticoids levels suppressing the occurrence of musth signals. In addition external environmental conditions affected hormone levels. The presence of receptive females resulted in elevated androgens in dominant musth males but increased glucocorticoids in subordinate non-musth males. The presented data on hormones, behavior and reproductive tactics strongly support an underlying endocrine mechanism for mediating the translation of intrinsic as well as extrinsic local conditions into the conditional dependent reproductive tactics in male elephants via interactions between the hypothalamic-pituitary-gonadal and -adrenal axes.     

Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (pisces: blenniidae)

In species in which intense intermale competition for the access to females is present males of lower competitive ability may adopt alternative reproductive tactics (ART) to get access to mates. These ART translate in many cases into male sexual polymorphism, with individuals following distinctly different tactics. Usually two alternative male morphs can be recognized in species with ART: (1) bourgeois males that compete for access to mates invest in typically male behaviors, such as building elaborated nests or displaying ornaments; and (2) parasitic males that take advantage of the success of the bourgeois males in attracting females and attempt "sneaker" fertilizations (e.g., sneaker and satellite males). In combtooth blennies (Blenniidae) the co-occurrence of ART and male sexual polymorphism has been described for two temperate species: the peacock blenny, Salaria pavo, and the Azorean rock-pool blenny, Parablennius sanguinolentus parvicornis. Interestingly, while in the peacock blenny the alternative male morph adopts a sneaker tactic, in the rock-pool blenny parasitic males act as satellites to nest-holder males. Thus, this variation in the ART expressed in these two closely related species allows for a comparative study of the proximate and ultimate factors affecting the expression of the two ART. In this article we summarize the available information on androgen levels in bourgeois and parasitic males of natural populations of the two species and of recent studies on the effect of exogenous administration of androgens on tactic switching in parasitic males of the two species. The information is discussed within the frame of the relative plasticity hypothesis, which predicts that plastic alternative morphs should show differences in hormone levels and that the administration of sex steroids should be effective in promoting the switch from the parasitic to bourgeois tactic. The evidence is only partly consistent with this hypothesis. Alternatively, a social transduction hypothesis that better fits the available data on androgens and ART in teleost is proposed. It states that the observed differences in androgen levels between alternative morphs should not be interpreted as an organization vs activation effect of steroids, but rather as the limited vs lifelong responsiveness of the neuroendocrine axis to social regulation.     

The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes

Among vertebrate classes, fishes exhibit by far the greatest variability in competitive and cooperative behaviors in male reproduction. Scramble competition between reproductive males is one possibility. Another possibility occurs when resources, mates, or locations can be monopolized, in which case males may invest in primary access to fertilizations by adopting a "bourgeois" strategy, or they may employ alternative mating tactics to evade the reproductive monopoly of other males. Adaptations in morphology, physiology, and behavior to bourgeois and alternative phenotypes are highly divergent. Here I review the functional characteristics that differ between bourgeois and parasitic phenotypes, and discuss the variability of alternative reproductive tactics at the levels of plasticity, determination, and selection. Examples will illustrate the importance of ecology, and will suggest that variation in reproductive tactics is largely adaptive. Behavioral solutions to competition for mates and fertilizations often involve agonistic behavior and conflict, but also cooperation among competitors (e.g., when subordinate males pay a price to bourgeois males for gaining access to fertilizable eggs). Application of molecular genetic tools has helped to uncover intricate sexual and social relationships in various fish species, including species that display some of the most complex reproductive and social patterns known among the vertebrates.     

Tactic-dependent plasticity in ejaculate traits in the swordtail Xiphophorus nigrensis

In species with alternative reproductive tactics, males that sneak copulations often have larger, higher quality ejaculates relative to males that defend females or nest sites. Ejaculate traits can, however, exhibit substantial phenotypic plasticity depending on a male's mating role in sperm competition, which may depend on the tactic of his competitor. We tested whether exposure to males of different tactics affected sperm number and quality in the swordtail Xipophorus nigrensis, a species with small males that sneak copulations and large males that court females. Sperm swimming speed was higher when the perceived competitor was small than when the competitor was large. Plasticity, however, was only exhibited by small males. Sperm number and viability were invariant between social environments. Our results suggest sperm quality is role-dependent and that plastic responses to the social environment can differ between male reproductive tactics.     

Determinants of male fitness: disentangling intra- and inter-sexual selection

Both intra- and inter-sexual selection may crucially determine a male's fitness. Their interplay, which has rarely been experimentally investigated, determines a male's optimal reproductive strategy and thus is of fundamental importance to the understanding of a male's behaviour. Here we investigated the relative importance of intra- and inter-sexual selection for male fitness in the common lizard. We investigated which male traits predict a male's access to reproduction allowing for both selective pressures and comparing it with a staged mating experiment excluding all types of intra-sexual selection. We found that qualitatively better males were more likely to reproduce and that sexual selection was two times stronger when allowing for both selective pressures, suggesting that inter- and intra-sexual selection determines male fitness and confirming the existence of multi-factorial sexual selection. Consequently, to optimize fitness, males should trade their investment between the traits, which are important for inter- and intra-sexual selection.     

Sexual dimorphism,temporal niche differentiation,and evidence for the Jack Sprat effect in an annual dioecious plant

Sexual dimorphism in dioecious plants often occurs as a consequence of the different resource requirements of females and males, especially during reproduction. The contrasting reproductive roles of the sexes can influence the phenology of growth, plant size, and flowering time, with implications for the intensity of competitive interactions within and between the sexes. Here, we investigate the influence of contrasting nutrient regimes and intra-sexual and inter-sexual competition on the expression of sexual dimorphism in life-history traits and biomass allocation throughout the life cycle of the dioecious annual Rumex hastatulus Baldw. (Polygonaceae). Development of a sex-specific marker enabled us to quantify the influence of competition on sex-specific differences in mortality and vegetative traits. We were particularly interested in determining whether the overall performance of the sexes might differ between the two forms of intra-specific competition, potentially providing evidence for sexual specialization in resource acquisition and niche differentiation. Our results indicated that although patterns of sexual dimorphism were dynamic, they were largely insensitive to nutrient conditions. We found that intra-sexual competition was more severe than inter-sexual competition, differentially affecting mortality and most traits during the vegetative and particularly the reproductive stage of the life history. Female trait values generally increased more under inter-sexual than intra-sexual competition in comparison to males. Our findings are consistent with temporal niche differentiation resulting from sexual specialization for different resource requirements and provide evidence for the “Jack Sprat effect.”     

Cognitive ability is heritable and predicts the success of an alternative mating tactic

The ability to attract mates, acquire resources for reproduction, and successfully outcompete rivals for fertilizations may make demands on cognitive traits—the mechanisms by which an animal acquires, processes, stores and acts upon information from its environment. Consequently, cognitive traits potentially undergo sexual selection in some mating systems. We investigated the role of cognitive traits on the reproductive performance of male rose bitterling (Rhodeus ocellatus), a freshwater fish with a complex mating system and alternative mating tactics. We quantified the learning accuracy of males and females in a spatial learning task and scored them for learning accuracy. Males were subsequently allowed to play the roles of a guarder and a sneaker in competitive mating trials, with reproductive success measured using paternity analysis. We detected a significant interaction between male mating role and learning accuracy on reproductive success, with the best-performing males in maze trials showing greater reproductive success in a sneaker role than as a guarder. Using a cross-classified breeding design, learning accuracy was demonstrated to be heritable, with significant additive maternal and paternal effects. Our results imply that male cognitive traits may undergo intra-sexual selection.     

Alternative reproductive tactics in snail shell‐brooding cichlids diverge in energy reserve allocation

Life history theory predicts that the amount of resources allocated to reproduction should maximize an individual's lifetime reproductive success. So far, resource allocation in reproduction has been studied mainly in females. Intraspecific variation of endogenous energy storage and utilization patterns of males has received little attention, although these patterns may vary greatly between individuals pursuing alternative reproductive tactics (ARTs). ARTs are characterized by systematic variation of behavioral, physiological, and often morphological traits among same‐sex conspecifics. Some individuals may rely on previously accumulated reserves, because of limited foraging opportunities during reproduction. Others may be able to continue foraging during reproduction, thus relying on reserves to a lesser extent. We therefore predicted that, if male tactics involve such divergent limitations and trade‐offs within a species, ARTs should correspondingly differ in energy reserve allocation and utilization. To test this prediction, we studied short‐term and long‐term reserve storage patterns of males in the shell‐brooding cichlid Lamprologus callipterus. In this species, bourgeois males investing in territory defense, courtship, and guarding of broods coexist with two distinct parasitic male tactics: (1) opportunistic sneaker males attempting to fertilize eggs by releasing sperm into the shell opening when a female is spawning; and (2) specialized dwarf males attempting to enter the shell past the spawning female to fertilize eggs from inside the shell. Sneaker males differed from other male types by showing the highest amount of accumulated short‐term and long‐term fat stores, apparently anticipating their upcoming adoption of the nest male status. In contrast, nest males depleted previously accumulated energy reserves with increasing nest holding period, as they invest heavily into costly reproductive behaviors while not taking up any food. This conforms to a capital breeder strategy. Dwarf males did not accumulate long‐term fat stores at all, which they can afford due to their small behavioral effort during reproduction and their continued feeding activity, conforming to an income breeder strategy. Our data confirm that the resource storage patterns of males pursuing ARTs can diverge substantially, which adds to our understanding of the coexistence and maintenance of alternative reproductive patterns within species.     

Environmental and endocrine correlates of tactic switching by nonterritorial male tree lizards (Urosaurus ornatus)

Animals often exhibit individual variation in their behavioral responses to the same stimuli in the biotic or abiotic environment. To elucidate the endocrine mechanisms mediating such behavioral variation, we have been studying a species of lizard with two distinct male phenotypes. Here we document behavioral variation across years in one of the two male phenotypes of the tree lizard, Urosaurus ornatus, and present hormone data that support an endocrine mechanism underlying this behavioral variation. Nonterritorial male tree lizards appear to be nomadic rovers in some years and sedentary satellites in others, whereas territorial males are always territorial. This behavioral variation by nonterritorial males was correlated with environmental conditions. In environmentally harsher years (as assessed by rainfall), nonterritorial males appear to behave as nomads, whereas in more benign years they are more site-faithful. A between-year comparison of levels of corticosterone and testosterone for the two male phenotypes supports a model for how hormones underlie the males' reproductive tactics, particularly the nonterritorial males' behavioral plasticity. In an environmentally harsher (drier) year, both types of males had higher corticosterone levels than in a milder (wetter) year, but only nonterritorial males had lower testosterone in the relatively harsher year. We propose that disruptive selection for individual variation in hormonal responses to environmental cues may be a common mechanism underlying the evolution of alternative male reproductive tactics in this and other species.     

Reproductive strategies in snakes

Snakes of both sexes display remarkable flexibility and diversity in their reproductive tactics. Many features of reproduction in female snakes (such as reproductive mode and frequency, seasonality and multiple mating) allow flexible maternal control. For example, females can manipulate not only the genotypes of their offspring (through mate choice or enhanced sperm competition) but also the phenotypes of their offspring (through allocation 'decisions', behavioural and physiological thermoregulation, and nest-site selection). Reliance on stored energy ('capital') to fuel breeding results in low frequencies of female reproduction and, in extreme cases, semelparity. A sophisticated vomeronasal system not only allows male snakes to locate reproductive females by following scent trails, but also facilitates pheromonally mediated mate choice by males. Male-male rivalry takes diverse forms, including female mimicry and mate guarding; combat bouts impose strong selection for large body size in males of some species. Intraspecific (geographical) variation and phenotypic plasticity in a wide array of reproductive traits (offspring size and number; reproductive frequency; incidence of multiple mating; male tactics such as mate guarding and combat; mate choice criteria) provide exceptional opportunities for future studies.     

Androgens and Immune Function in Male Alternative Reproductive Morphotypes of the Peacock Blenny Salaria pavo

Species with alternative reproductive tactics offer the opportunity to analyse how behavioural and morphological traits are tuned to produce successfully competing phenotypes within one sex. In the teleost fish Salaria pavo , alternative reproductive tactics are sequential. The older ornamented males compete for access to females by guarding a cavity to which they attract females to spawn. Ornamented males that are found without a nest are called 'floaters'. Younger mature males which are too small to compete with nest-holders attempt to 'sneak' as female mimics into successful nests and release their sperm to fertilize freshly spawned eggs. The alternative tactics in S. pavo are associated with different levels of the androgens testosterone and 11-ketotestosterone, which have been found to suppress immune function in several teleost fish. A field study was carried out to analyse the relationship between these reproductive tactics, androgens and blood levels of lymphocytes as a monitoring method of immune function. We expected highest investment in the immune system in sneakers because these have the lowest androgen levels and functionally because investing in self-maintenance increases their future prospect to switch tactic and to reproduce as a nest-holder. Indeed, the relative count of lymphocytes correlated negatively with body size and thus was highest in sneakers and lowest in nest-holders. In concordance, 11-ketotestosterone and testosterone levels were found to be higher in floaters and nest-holders than in sneakers. However, no correlation was found between individual levels of testosterone or 11-ketotestosterone and lymphocytes. Thus, a trade-off between reproductive traits associated with high androgen levels and immunocompetence might exist at the level of alternative tactics but this might not be explained by acute immunosuppressive effects of circulating androgens.     

Ownership-dependent mating tactics of minor males of the beetle <Emphasis Type="Italic">Librodor japonicus</Emphasis> (Nitidulidae) with intra-sexual dimorphism of mandibles

Intra-sexual dimorphism is found in the weapons of many male beetles. Different behavioral tactics to access females between major and minor males, which adopt fighting and alternative tactics, respectively, are thought to maintain the male dimorphism. In these species major males have enlarged weapons that they use in fights with rival males. Minor males also have small weapons in some of these species, and it is unclear why these males possess weapons. We examined the hypothesis that minor males might adopt a fighting tactic when their status was relatively high in comparison with that of other males (e.g., ownership of a territory). We observed the behavioral tactics of major and minor males of the beetle Librodor japonicus, whose males have a dimorphism of their mandibles. Major males fought for resources, whereas minor males adopted two status-dependent tactics, fighting and sneaking, to access females, depending on their ownership of a sap site. We suggest that ownership status-dependent mating tactics in minor males may maintain the intra-sexual dimorphism in this beetle.     

Reproductive endocrinology of zoo-housed aardwolves

Knowledge regarding the relationship between endocrine parameters and reproductive activity can offer important insights into how social and environmental factors influence the reproductive success of mammals. Although components of both the physical and social environment affect endocrine regulation of reproduction, less is understood about the potential role of interactions between different endocrine axes on reproductive activity. We evaluated temporal patterns of reproductive and adrenocortical steroids in two male and three female aardwolves (Proteles cristata) housed in captivity at Brookfield Zoo, Chicago, IL, USA. We found seasonal variation in faecal androgens, estrogens, and progestagens, which provide support for previous observations of the aardwolf as a seasonal breeder. However, the timing of peak endocrine activity did not correspond to observations from wild populations. Our interpretation is that this discrepancy is caused by photoperiodic regulation of reproductive activity. We found a positive relationship between faecal androgens and faecal glucocorticoid metabolites in males and a positive relationship between faecal estrogens and faecal glucocorticoid metabolites in females when housed with conspecifics but not when housed alone. We also found a positive but asymptotic relationship between faecal progestagens and faecal glucocorticoid metabolites. We argue that these observations indicate a potential effect of reproductive endocrine activity on the hypothalamic–pituitary–adrenal axis, which could result in interesting physiological trade-offs in male reproductive tactics and female pre-partum maternal investment because of the negative effects of long-term glucocorticoid elevation on reproductive performance. Finally, our results suggest that social and environmental factors interact in regulating many aspects of endocrine fluctuations in this mostly solitary species.     

Sex,androgens, and whole‐organism performance in an Australian lizard

Understanding underlying physiological differences between the sexes in circulating androgens and how hormonal variation affects morphology–performance relationships may help clarify the evolution of sexual dimorphism in diverse taxa. Using a widely distributed Australian lizard (Eulamprus quoyii) with weak sexual dimorphism and no dichromatism, we tested whether circulating androgens differed between the sexes and whether they covaried with morphological and performance traits (bite force, sprint speed, endurance). Males had larger head dimensions, stronger bite force, faster sprint speed, and longer endurance compared to females. We found that the sexes did not differ in androgen concentrations and that androgens were weakly associated with both morphological and performance traits. Interestingly, high circulating androgens showed a nonlinear relationship with bite force in males and not females, with this relationship possibly being related to alternative male reproductive tactics. Our results suggest that androgens are not strongly correlated with most performance and morphological traits, although they may play an important organizational role during the development of morphological traits, which could explain the differences in morphology and thus performance between the sexes. Differences in performance between the sexes suggest differential selection on these functional traits between males and females. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 834–849.     

Gonadotropin hormone modulation of testosterone, immune function, performance, and behavioral trade-offs among male morphs of the lizard Uta stansburiana

Sexual selection predicts that trade-offs maintain trait variation in alternative reproductive strategies. Experiments often focus on testosterone (T), but the gonadotropins follicle-stimulating hormone and luteinizing hormone may provide a clearer understanding of the pleiotropic relationships among traits. We assess the activational role of gonadotropins on T and corticosterone regulation in traits expressed by polymorphic male side-blotched lizards Uta stansburiana. Gonadotropins are found to enhance and suppress multiple physiological, morphological, and behavioral traits independently, as well as indirectly via T, and we demonstrate selective trade-offs between reproduction and survival. The OBY locus, a genetic marker in our model vertebrate mating system, allows characterization of the interaction between genotype and hormone treatment on male traits. Our results suggest that oo, ob, and bb males are near their physiological and behavioral capacity for reproductive success, whereas yy and by males are maintained below their physiological maximum. Both by and yy morphs show trait plasticity, and we demonstrate that gonadotropins are likely proximate effectors that govern not only trait differences between alternative mating strategies but also morph plasticity. Gonadotropins clearly represent an important mechanism maintaining variation in physiological, morphological, and behavioral traits, as well as potentially maintaining the immunosuppression costs of male sexual signals.     

Strategic female reproductive investment in response to male attractiveness in birds

Life-history theory predicts that individuals should adjust their reproductive effort according to the expected fitness returns on investment. Because sexually selected male traits should provide honest information about male genetic or phenotypic quality, females may invest more when paired with attractive males. However, there is substantial disagreement in the literature whether such differential allocation is a general pattern. Using a comparative meta-regression approach, we show that female birds generally invest more into reproduction when paired with attractive males, both in terms of egg size and number as well as food provisioning. However, whereas females of species with bi-parental care tend to primarily increase the number of eggs when paired with attractive males, females of species with female-only care produce larger, but not more, eggs. These patterns may reflect adaptive differences in female allocation strategies arising from variation in the signal content of sexually selected male traits between systems of parental care. In contrast to reproductive effort, female allocation of immune-stimulants, anti-oxidants and androgens to the egg yolk was not consistently increased when mated to attractive males, which probably reflects the context-dependent costs and benefits of those yolk compounds to females and offspring.     

Determinants and long‐term costs of early reproduction in males of a long‐lived polygynous mammal

In long‐lived polygynous species, male reproductive success is often monopolized by a few mature dominant individuals. Young males are generally too small to be dominant and may employ alternative tactics; however, little is known about the determinants of reproductive success for young males. Understanding the causes and consequences of variability in early reproductive success may be crucial to assess the strength of sexual selection and possible long‐term trade‐offs among life‐history traits. Selective pressures driven by fluctuating environmental conditions may depend on age class. We evaluated the determinants of reproduction in male bighorn sheep (Ovis canadensis) aged 2–4 years using 30 years of individual‐level data. These young males cannot defend estrous ewes and use alternative mating tactics. We also investigated how the age of first detected reproduction was correlated to lifetime reproductive success and longevity. We found that reproductive success of males aged 3 years was positively correlated to body mass, to the proportion of males aged 2–4 years in the competitor pool, and to the number of females available per adult male. These results suggest that reproductive success depends on both competitive ability and population age–sex structure. None of these variables, however, had significant effects on the reproductive success of males aged 2 or 4 years. Known reproduction before the age of five increased lifetime reproductive success but decreased longevity, suggesting a long‐term survival cost of early reproduction. Our analyses reveal that both individual‐level phenotypic and population‐level demographic variables influence reproductive success by young males and provide a rare assessment of fitness trade‐offs in wild polygynous males.