Endocrine correlates of alternative phenotypes in the white-throated sparrow (Zonotrichia albicollis)

Many vertebrate species exhibit alternative phenotypes (or morphs), in which one sex displays phenotypic variation equal to or greater than the variation between the sexes. Males in such species typically display differences in reproductive strategies and morphology. Steroid hormones such as testosterone are known modulators of reproductive behavior and morphology and therefore are obvious candidates for the mediation of phenotypic differences between morphs. We conducted a year-round study in the white-throated sparrow (Zonotrichia albicollis) that exhibits alternative phenotypes in plumage coloration and behavior in both sexes: during the breeding season, white-striped males and females are more aggressive and have higher song rates than tan-striped individuals. At the beginning of the breeding season, free-living white-striped males had higher plasma testosterone concentrations than tan-striped males. However, this finding might have been due to different social experiences because captive male morphs sampled at similar times of year did not differ in testosterone concentrations. Captive white-striped males had larger testis and cloacal protuberance sizes than tan-striped males, which might be related to the divergent mating strategies of the morphs. Male morphs showed similar increases in luteinizing hormone following injections of gonadotropin-releasing hormone, but white-striped males showed larger increases in testosterone, indicating differences between morphs in gonadal testosterone production. Females had low concentrations of testosterone, and morphs did not differ. Plasma dehydroepiandrosterone (DHEA) concentrations were elevated in both sexes and morphs during the breeding and non-breeding seasons. These data do not support the hypothesis that testosterone activates behavioral differences between alternative phenotypes in the white-throated sparrow. Alternative testable hypotheses include hormonal effects during early development and direct genetic effects.     

An experimental test for alternative reproductive strategies underlying a female-limited polymorphism

Polymorphism often corresponds to alternative mating tactics in males, but much less is known about this relationship in females. However, recent work suggests that selection for alternative reproductive strategies in females can maintain genetic variation in important life-history traits. Brown anole lizards (Anolis sagrei) exhibit a genetically based polymorphism in dorsal pattern that is expressed only by females, which occur in bar (B), diamond (D) and intermediate diamond-bar (DB) morphs. Here, we use a combination of natural history data, captive breeding studies and phenotypic manipulations of reproductive investment to test the hypothesis that this polymorphism corresponds to morph-specific patterns of reproductive investment. Three years of data from wild females and two generations of captive breeding revealed no differences among morphs in the frequency of egg production or in the number, frequency, size or sex ratio of offspring. Manipulations of reproductive investment via surgical ovariectomy revealed significant costs of reproduction with respect to survival, growth, immune function and haematocrit, but the magnitudes of these costs did not differ among morphs. Collectively, our results refute the hypothesis that this sex-limited polymorphism is maintained by selection for alternative reproductive strategies. We compare this finding to other systems in which polymorphic females exhibit alternative reproductive tactics and discuss other selective factors that could maintain polymorphism in anoles.     

Structural complexity of the environment affects the survival of alternative male reproductive tactics

Alternative reproductive tactics in males are often associated with divergent phenotypes expressed as phenotypically plastic threshold traits. The evolution of threshold traits in these species has been modeled under the conditional evolutionarily stable strategy (ESS). Both strategic and genetic models predict that perturbations to the fitness trade-off between the male morphs will lead to a shift in the ESS switch point of the threshold. So far, demographic factors that influence the competitive ability of male morphs have been investigated and related to intraspecific population variation in male dimorphic thresholds. Here we reveal evidence for the theoretical prediction that abiotic features of the environment, in particular its structural complexity, are likely to influence the ESS threshold. In the male dimorphic mite Sancassania berlesei, we monitored the survival of aggressive fighter males and their benign scrambler counterparts in populations that differed in structural complexity. We found that, consistent with our prediction, the complex habitat favored fighter males, enabling them to kill a greater number of rival scramblers. We found no effect of habitat complexity on the survival of fighter males. These results demonstrate how abiotic as well as biotic aspects of the environment can be important in determining the frequencies of males adopting alternative tactics in different species or populations.     

Intralocus tactical conflict: genetic correlations between fighters and sneakers of the dung beetle Onthophagus taurus

Males and females differ in their phenotypic optima for many traits, and as the majority of genes are expressed in both sexes, some alleles can be beneficial to one sex but harmful to the other (intralocus sexual conflict; ISC). ISC theory has recently been extended to intrasexual dimorphisms, where certain alleles may have opposite effects on the fitness of males of different morphs that employ alternative reproductive tactics (intralocus tactical conflict; ITC). Here, we use a half‐sib breeding design to investigate the genetic basis for ISC and ITC in the dung beetle Onthophagus taurus. We found positive heritabilities and intersexual genetic correlations for almost all traits investigated. Next, we calculated the intrasexual genetic correlation between males of different morphs for horn length, a sexually selected trait, and compared it to intrasexual correlations for naturally selected traits in both sexes. Intrasexual genetic correlations did not differ significantly between the sexes or between naturally and sexually selected traits, failing to support the hypothesis that horns present a reduction of intrasexual genetic correlations due to ITC. We discuss the implications for the idea of developmental reprogramming between male morphs and emphasize the importance of genetic correlations as constraints for the evolution of dimorphisms.     

Body Size and Morph as Drivers of Copulation Duration in a Male Dimorphic Damselfly

Copulation duration is often highly variable within and among species. Here, we explore the roles of body size, male morph, morph frequency, and alternative reproductive tactics to explain copulation duration in the damselfly Paraphlebia zoe. P. zoe has two male morphs (pigmented or hyaline wings) which differ in reproductive tactics (territorial or non‐territorial behaviors). We also analyze the effects of season as the frequencies of both morphs tend to vary along the reproductive season. In the first non‐experimental year, we found that the relationship between body size and copulation duration depended on the time of year. Early in the season, body size positively correlated with copulation duration, while late in the year, body size negatively correlated with copulation duration. In the second experimental year (when we reversed the frequency of male morphs in the middle of the season: making pigmented males less frequent than hyaline males), size influenced copulation duration as well as morph – body size positively correlated with copulation duration, and hyaline males mated for longer than pigmented males. Contrary to our prediction, changes to the relative abundances of morphs did not influence copulation duration. Hyaline males may be under selection for longer copulation durations to compensate for their reduced access to females, as long copulations potentially lead to more rival sperm to be removed from the female sperm storage organs and/or increased mate guarding. We do not discard, however, other explanations that drive variation in copulation duration such as cryptic female choice and/or predation.     

Behavioral and hormonal correlates of alternative reproductive strategies in a polygynous lizard: Tests of the relative plasticity and challenge hypotheses

Species with alternative reproductive tacts are good models to investigate the poorly understood question of whether individual variation within sexes results from the same physiological mechanisms that control variation between sexes. We have shown previously that adult male tree lizards, Urosaurus ornatus, of different throat color morphs express different levels of aggression in the laboratory. Further field results support the suggestion that the two morphs practice alternative reproductive tactics because the two morphs express different levels of aggressive behavior under field conditions and exhibit dramatic and opposite responses to aggressive challenges. However, despite these behavioral differences, the two morphs do not differ in levels of testosterone or corticosterone either in undisturbed situations or following aggressive challenge. These results are consistent with the relative plasticity hypothesis which proposes that organizational, rather than activational, actions of steroid hormones will be more important in morph differentiation when morphs are fixed in adult life, as they are in tree lizards. These results also support the hypothesis that steroid hormonal levels are insensitive to social modulation in males of species such as U. ornatus without paternal care.     

Alternative reproductive strategies and the maintenance of female color polymorphism in damselflies

Genetic polymorphisms are powerful model systems to study the maintenance of diversity in nature. In some systems, polymorphisms are limited to female coloration; these are thought to have arisen as a consequence of reducing male mating harassment, commonly resulting in negative frequency‐dependent selection on female color morphs. One example is the damselfly Ischnura elegans, which shows three female color morphs and strong sexual conflict over mating rates. Here, we present research integrating male tactics, and female evolutionary strategies (female mating behavior and morph‐specific female fecundity) in populations with different morph‐specific mating frequencies, to obtain an understanding of mating rates in nature that goes beyond the mere measure of color frequencies. We found that female morph behavior differed significantly among but not within morphs (i.e., female morph behavior was fixed). In contrast, male tactics were strongly affected by the female morph frequency in the population. Laboratory work comparing morph‐specific female fecundity revealed that androchrome females have lower fecundity than both of the gynochrome female morphs in the short term (3‐days), but over a 10‐day period one of the gynochrome female morphs became more fecund than either of the other morphs. In summary, our study found sex‐specific dynamics in response to different morph frequencies and also highlights the importance of studying morph‐specific fecundities across different time frames to gain a better understanding of the role of alternative reproductive strategies in the maintenance of female‐limited color polymorphism.     

An experimental investigation into status-dependent male dimorphism in the European earwig, Forficula auricularia

Discrete alternative reproductive phenotypes are probably often due to individuals adopting alternative tactics with unequal fitnesses in conditional strategies with status-dependent selection. One tactic is believed to be favoured below a status switch point and another tactic above it, owing to different fitness functions of the tactics. Males of the European earwig are dimorphic. Macrolabic males are large (high status) and have long forceps, and brachylabic males are small (low status) with short forceps. I tested whether fitness functions, measured as mating success, of the two morphs differed with regard to forceps length and body weight. Macrolabic males with longer forceps than a competing male had higher mating success but brachylabic males benefited by being heavier than their competitor. Thus, different selection regimes were acting on the two morphs, suggesting that their fitness functions differed in relation to status. These observations and those of previous studies, showing that morph expression is environmentally determined and is associated with body size and that the morphs have unequal fitness, provide support for the hypothesis that male dimorphism in this species is a conditional strategy that has evolved under status-dependent selection. The differential investment in forceps growth that characterizes the morphs was manifested in a steeper allometric relation between forceps length and body size in macrolabic than brachylabic males. Behavioural observations showed that males of both morphs engaged in direct contests for females. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

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.     

SELECTION FOR ALTERNATIVE MALE REPRODUCTIVE TACTICS ALTERS INTRALOCUS SEXUAL CONFLICT

Intralocus sexual conflict (IASC) arises when fitness optima for a shared trait differ between the sexes; such conflict may help maintain genetic variation within populations. Sex‐limited expression of sexually antagonistic traits may help resolve the conflict, but the extent of this resolution remains a subject of debate. In species with alternative male reproductive tactics, unresolved conflict should manifest more in a more sexually dimorphic male phenotype. We tested this prediction in the bulb mite (Rhizoglyphus robini), a species in which aggressive fighters coexist with benign scramblers. To do this, we established replicated lines in which we increased the proportion of each of the alternative male morphs using artificial selection. After approximately 40 generations, the proportion of fighters and scramblers stabilized at >0.9 in fighter‐ and scrambler‐selected lines, respectively. We then measured several female fitness components. As predicted by IASC theory, female fecundity and longevity were lower in lines selected for fighters and higher in lines selected for scramblers. This finding indicates that sexually selected phenotypes are associated with an ontogenetic conflict that is not easily resolved. Furthermore, we suggest that IASC may be an important mechanism contributing to the maintenance of genetic variation in the expression of alternative reproductive tactics.     

Dimorphic Males Display Alternative Reproductive Strategies in the Marine Amphipod Jassa marmorata Holmes (Corophioidea: Ischyroceridae)

Discrete dimorphism of males within a species is often the result of selection for alternative reproductive strategies, and these strategies may be evolutionarily stable (ESS). An ESS may be either mixed (genetically fixed differences) or conditional (flexible differences related to varying environmental conditions) (PARKER 1984). Mature males of the marine amphipod Jassa marmorata are dimorphic. Large ‘major’ males have a greatly enlarged thumb (propodus) on their 2nd gnathopods, while small ‘minor’ males exhibit thumbs that are reduced, and CONIAN (1989) suggested that minors may exhibit a different mating strategy from majors. Ratios of males and females fluctuate seasonally (FRANZ 1989) and female body size is inversely correlated with temperature (FRANZ 1989) so male dimorphism could be a flexible response to varying environmental conditions. I sampled a natural population of J. marmorata over a 1-yr period, quantified major and minor morphology, and measured male behaviour and mating success in experimental arenas that contained varying proportions of male morphs and females. Morphology of the two morphs is discrete; female body size varies with season with significantly smaller individuals in summer and fall; body size predicts morph type; and ratios of majors, minors and females fluctuate seasonally. Finally I showed that majors and minors use different mating tactics to gain access to receptive females, and that these behaviours depend on the male's own morphology and on the environmental setting that it finds itself in. Major males fight, display and attempt to evict other males to mate with receptive females. Minors never fight with, display to or attempt to evict majors, but they infrequently display to and attempt to evict other minor males. Furthermore, mating success of the two morphs was not significantly different and may depend on whether males are with a majority or minority of their own type. These data support the conclusion that major and minor male J. marmorata display evolutionarily stable alternative reproductive strategics, but more work should address the nature of this ESS.     

Breeding success of male brook trout (Salvelinus fontinalis) in the wild

Competition for females generally results in some males adopting alternative reproductive tactics to acquire matings. For fish, the ecological and evolutionary consequences of these tactics are not well understood because of an inability to link directly the interactions of individuals on the breeding grounds with genetic data. This study combines behavioural observations with genetic estimates of male reproductive success within an intensively studied wild population of lacustrine brook trout (Salvelinus fontinalis). Male brook trout exhibit a conditional reproductive strategy with small males adopting a peripheral position to that of larger dominant males in their proximity to spawning females. Parentage analysis of eggs collected from wild redds confirmed the reproductive success of individual males. Males relegated to peripheral positions during spawning participated frequently in spawning events, but in most cases the first male to spawn was the sole contributor, and no more than two males contributed successfully to a single brood. While behavioural observations of salmonines suggests that reproduction is partitioned among males in a manner dependent upon body size and proximity to spawning females, the genetic evidence from this study suggests a more limited distribution of reproductive success in the field. The genetic contributions of male brook trout are highly skewed towards larger males for this population. A review of the salmonine literature suggests little difference in individual reproductive success for males exhibiting size-related tactics within a conditional mating strategy vs. precocial maturation. Collectively, these genetic studies provide new insights on the evolution of alternative life histories among salmonines.     

Do individuals in better condition survive for longer? Field survival estimates according to male alternative reproductive tactics and sex

There is a gap in terms of the supposed survival differences recorded in the field according to individual condition. This is partly due to our inability to assess survival in the wild. Here we applied modern statistical techniques to field‐gathered data in two damselfly species whose males practice alternative reproductive tactics (ARTs) and whose indicators of condition in both sexes are known. In Paraphlebia zoe, there are two ART: a larger black‐winged (BW) male which defends mating territories and a smaller hyaline‐winged (HW) male that usually acts as a satellite. In this species, condition in both morphs is correlated with body size. In Calopteryx haemorrhoidalis, males follow tactics according to their condition with males in better condition practicing a territorial ART. In addition, in this species, condition correlates positively with wing pigmentation in both sexes. Our prediction for both species was that males practicing the territorial tactic will survive less longer than males using a nonterritorial tactic, and larger or more pigmented animals will survive for longer. In P. zoe, BW males survived less than females but did not differ from HW males, and not necessarily larger individuals survived for longer. In fact, size affected survival but only when group identity was analysed, showing a positive relationship in females and a slightly negative relationship in both male morphs. For C. haemorrhoidalis, survival was larger for more pigmented males and females, but size was not a good survival predictor. Our results partially confirm assumptions based on the maintenance of ARTs. Our results also indicate that female pigmentation, correlates with a fitness component – survival – as proposed by recent sexual selection ideas applied to females.     

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.     

Colour Polymorphism and Alternative Breeding Strategies: Effects of Parent’s Colour Morph on Fitness Traits in the Common Wall Lizard

Colour polymorphism (CP) is widespread in animals, but mechanisms underlying morph evolution and maintenance are not completely resolved. In reptiles, CP is often genetically based and associated with alternative behavioural strategies, mainly in males for most cases. However, female colour morphs also display alternative reproductive strategies associated with behavioural and physiological traits, which may contribute to maintain CP in the population. Both sexes of the common wall lizard (Podarcis muralis) show three pure colour morphs, white, yellow and red. Here, we looked for the effects of male and female colour morphs on fitness traits of captive-breeding pairs. All yellow-throated females laid clutches of many small eggs and produced many light offspring, behaving as r-strategists, whereas white-throated females laid clutches of few large eggs and produced few heavy offspring, behaving as K-strategists. Red-throated females adopted a conditional Kr-strategy depending on their size/age. These basic female strategies were modulated in relation to mate morph: white females had the best fitness gain in terms of viable offspring when mated to red males; mating between yellow morphs yielded a greater breeding success than all other morph crosses, but also lighter offspring; finally, red females produced heavy progeny when paired with red or white males, and light offspring in pair with yellow males. Thus, correlation between CP and traits relevant to fitness combined with non-random mating, either assortative or disassortative, could increase the potential for CP to contribute to divergent evolution in the common wall lizard.     

Space use and genetic structure do not maintain color polymorphism in a species with alternative behavioral strategies

Space use including territoriality and spatial arrangement within a population can reveal important information on the nature, dynamics, and evolutionary maintenance of alternative strategies in color polymorphic species. Despite the prevalence of color polymorphic species as model systems in evolutionary biology, the interaction between space use and genetic structuring of morphs within populations has rarely been examined. Here, we assess the spatial and genetic structure of male throat color morphs within a population of the tawny dragon lizard, Ctenophorus decresii. Male color morphs do not differ in morphology but differ in aggressive and antipredator behaviors as well as androgen levels. Despite these behavioral and endocrine differences, we find that color morphs do not differ in territory size, with their spatial arrangement being essentially random with respect to each other. There were no differences in genetic diversity or relatedness between morphs; however, there was significant, albeit weak, genetic differentiation between morphs, which was unrelated to geographic distance between individuals. Our results indicate potential weak barriers to gene flow between some morphs, potentially due to nonrandom pre‐ or postcopulatory mate choice or postzygotic genetic incompatibilities. However, space use, spatial structure, and nonrandom mating do not appear to be primary mechanisms maintaining color polymorphism in this system, highlighting the complexity and variation in alternative strategies associated with color polymorphism.     

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.     

Morph-dependent resource acquisition and fitness in a polymorphic bird

Understanding genetic colour polymorphism has proved a major challenge, both in terms of the underlying genetic mechanisms and the evolutionarily forces maintaining such genetic variation. In this context, genetic differences in aggression or competitive-related traits may covary with the expression of alternative phenotypes, and affect the evolutionary stability and maintenance of colour polymorphisms. Genetic red and black head-colour morphs of the Gouldian finch (Erythrura gouldiae) co-occur in temporally and geographically stable frequencies in sympatric populations. Gouldian finches are obligate cavity-nesters with highly specific preferences for nest-site morphometry that directly affect reproductive success. Because intra- and interspecific competition for high quality nest-sites is prevalent, and fitness is directly related to nest-site quality, we investigated the relative access (and consequences for reproductive success) of alternative morphs to this critical limiting resource in the wild. Red males defended higher quality nest-sites, and overcame greater levels of nest-site competition against conspecifics and superior heterospecific competitors than black males. Red-headed males also produced more fledglings (especially with red-headed females) than black-headed males, independent of nest-site quality. Finally, the independent (positive) effect of nest-site quality on reproductive success was confirmed. Such competitive asymmetries are important to relative selection among coexisting morphs, and are likely to contribute to the maintenance of alternative sympatric colour-morphs in wild populations.     

Performance capacity, fighting tactics and the evolution of life-stage male morphs in the green anole lizard (Anolis carolinensis)

The evolution of alternative male phenotypes is probably driven by male-male competition for access to reproductive females, but few studies have examined whether whole-organism performance capacities differ between male morphs, and if so whether any such differences affect fighting ability. We show how ontogenetic changes in performance and morphology have given rise to two distinct life-stage male morphs exhibiting different fighting tactics within the green anole lizard (Anolis carolinensis). Field studies show a bimodal distribution of adult males within a single population: larger 'heavyweight' males have relatively large heads and high bite forces for their size, whereas smaller 'lightweight' males have smaller heads and lower bite forces. In staged fights between size-matched heavyweight males, males with greater biting ability won more frequently, whereas in lightweight fights, males with greater jumping velocity and acceleration won more often. Because growth in reptiles is indeterminate, and the anole males examined are sexually mature, we propose that the heavyweight morph arose through selection against males with small heads and poor bite forces at the lightweight-heavyweight size transition. Our findings imply that one may not be able to predict male fighting success (and hence potential mating success) by examining aspects of male 'quality' at only one life stage.