Intrasexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish

The maintenance of colour polymorphisms within populations has been a long-standing interest in evolutionary ecology. African cichlid fish contain some of the most striking known cases of this phenomenon. Intrasexual selection can be negative frequency dependent when males bias aggression towards phenotypically similar rivals, stabilizing male colour polymorphisms. We propose that where females are territorial and competitive, aggression biases in females may also promote coexistence of female morphs. We studied a polymorphic population of the cichlid fish Neochromis omnicaeruleus from Lake Victoria, in which three distinct female colour morphs coexist: one plain brown and two blotched morphs. Using simulated intruder choice tests in the laboratory, we show that wild-caught females of each morph bias aggression towards females of their own morph, suggesting that females of all three morphs may have an advantage when their morph is locally the least abundant. This mechanism may contribute to the establishment and stabilization of colour polymorphisms. Next, by crossing the morphs, we generated sisters belonging to different colour morphs. We find no sign of aggression bias in these sisters, making pleiotropy unlikely to explain the association between colour and aggression bias in wild fish, which is maintained in the face of gene flow. We conclude that female-female aggression may be one important force for stabilizing colour polymorphism in cichlid fish.     

The evolution of alternative mating strategies in variable environments

Summary We assessed the influence of phenotypic plasticity in age at maturity on the maintenance of alternative mating strategies in male Atlantic salmon,Salmo salar. We calculated the fitness,r, associated with the parr and the anadromous strategies, using age-specific survival data from the field and strategy-specific fertilization data from the laboratory. The fitness of each strategy depended largely on mate competition (numbers of parr per female, i.e. parr frequency) and on age at maturity. Fitness declined with increasing numbers of parr per female with equilibrium frequencies (at which the fitnesses of each strategy are equal) being within the range observed in the wild. Equilibrium parr frequencies declined with decreasing growth rate and increasing age at maturity. Within populations, the existence of multiple age-specific sets of fitness functions suggests that the fitnesses of alternative strategies are best represented as multidimensional surfaces. The points of intersection of these surfaces, whose boundaries encompass natural variation in age at maturity and mate competition, define an evolutionarily stable continuum (ESC) of strategy frequencies along which the fitnesses associated with each strategy are equal. We propose a simple model that incorporates polygenic thresholds of a largely environmentally-controlled trait (age at maturity) to provide a mechanism by which an ESC can be maintained within a population. An indirect test provides support for the prediction that growth-rate thresholds for parr maturation exist and are maintained by stabilizing selection. Evolutionarily stable continua, maintained by negative frequency-dependent selection on threshold traits, provide a theoretical basis for understanding how alternative life histories can evolve in variable environments.     

Environment-contingent sexual selection in a colour polymorphic fish

Sexual selection could be a driving force in the maintenance of intraspecific variation, but supporting observations from nature are limited. Here, we test the hypothesis that spatial heterogeneity of the visual environment can influence sexual selection on colourful male secondary traits such that selective advantage is environment contingent. Using a small fish endemic to Sulawesi, Indonesia (Telmatherina sarasinorum) that has five male colour morphs varying in frequency between two visually distinct mating habitats, we used direct behavioural observations to test the environment-contingent selection hypothesis. These observations were combined with measurements of the visual environment, fish coloration and the sensitivity of visual photopigments to determine whether differential morph conspicuousness was associated with reproductive success across habitats. We found that blue and yellow males are most conspicuous in different habitats, where they also have the highest reproductive fitness. A less conspicuous grey morph also gained high reproductive success in both habitats, raising the possibility that alternative behaviours may also contribute to reproductive success. In a comprehensive analysis, conspicuousness was strongly correlated with reproductive success across morphs and environments. Our results suggest an important role for spatially heterogeneous environments in the maintenance of male colour polymorphism.     

Intrasexual selection and male mating strategies in baboons and macaques

If baboon and macaque mating systems constitute a form of female defense polygyny, male mating strategies should be intrasexually selected and should vary in predictable ways with female defensibility, and demographic factors which affect the numbers of competing males per estrous female in populations. Substantial behavioral evidence exists for intrasexual selection of male mating strategies in baboons and macaques. Limited evidence also offers tentative support for theorybased predictions about the relationship between male mating strategy and female defensibility. Although male dominance rank generally predicts mating success, there are a number of factors which tend to increase the success of subordinate males above that expected from a simple dominance-based model of priority of access to mates.     

Testing the role of coadapted genes versus bet-hedging for mating strategies in colour polymorphic pygmy grasshoppers

Recent investigations of mate choice indicate that the genetic effect of sires on offspring fitness may depend on the interaction between maternal and paternal genotypes and the environmental conditions experienced by the offspring. Alternative colour morphs of the pygmy grasshopper, Tetrix subulata , represent ecological strategies that differ in body size, life history, thermoregulatory behaviour, and habitat selection. The hypothesis that selection promotes behaviours maintaining coadapted gene complexes predicts individuals to mate assortatively with respect to colour morph. On the other hand, the bet-hedging hypothesis predicts that the temporal variability of the environment inhabited by these animals may select for disassortative mating behaviour resulting in heterogeneous offspring. To distinguish between these competing hypotheses, we investigated mating behaviours using dual-choice experiments. Our results were not in agreement with the prediction of assortative mating but suggest instead that matings were random with regard to colour morph. Polyandry was common, and females mated with the second male regardless of whether the first mating was assortative or disassortative. Polyandry also was equally frequent among females in triads in which the two males belonged to different colour morphs as in triads where both males belonged to the same colour morph. A field experiment confirmed that polyandry occurred also among free-ranging individuals, and uncovered variation in mating success among male colour morphs, probably due to indirect effects of coloration on activity or habitat use. The consequences of this random and polyandrous mating strategy for the evolutionary dynamics of the colour polymorphism remain to be explored.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 491–499.     

Endocrine differences among colour morphs in a lizard with alternative behavioural strategies

Alternative behavioural strategies of colour morphs are expected to associate with endocrine differences and to correspond to differences in physical performance (e.g. movement speed, bite force in lizards); yet the nature of correlated physiological and performance traits in colour polymorphic species varies widely. Colour morphs of male tawny dragon lizards Ctenophorus decresii have previously been found to differ in aggressive and anti-predator behaviours. We tested whether known behavioural differences correspond to differences in circulating baseline and post-capture stress levels of androgen and corticosterone, as well as bite force (an indicator of aggressive performance) and field body temperature. Immediately after capture, the aggressive orange morph had higher circulating androgen than the grey morph or the yellow morph. Furthermore, the orange morph maintained high androgen following acute stress (30 min of capture); whereas androgen increased in the grey and yellow morphs. This may reflect the previously defined behavioural differences among morphs as the aggressive response of the yellow morph is conditional on the colour of the competitor and the grey morph shows consistently low aggression. In contrast, all morphs showed an increase in corticosterone concentration after capture stress and morphs did not differ in levels of corticosterone stress magnitude (CSM). Morphs did not differ in size- and temperature-corrected bite force but did in body temperature at capture. Differences in circulating androgen and body temperature are consistent with morph-specific behavioural strategies in C. decresii but our results indicate a complex relationship between hormones, behaviour, temperature and bite force within and between colour morphs.     

Multiple signaling functions of song in a polymorphic species with alternative reproductive strategies

Vocal traits can be sexually selected to reflect male quality, but may also evolve to serve additional signaling functions. We used a long‐term dataset to examine the signaling potential of song in dimorphic white‐throated sparrows (Zonotrichia albicollis). We investigated whether song conveys multifaceted information about the vocalizing individual, including fitness, species identity, individual identity, and morph. We also evaluated whether song traits correlate differently with fitness in the two morphs, as the more promiscuous strategy of white, relative to tan, morph males might impose stronger sexual selection. Males with high song rates achieved higher lifetime reproductive success, and this pattern was driven by white morph males. In addition, males that sang songs with many notes survived longer, but this pattern was less robust. Thus, song traits reflect differences in fitness and may more strongly affect fitness in the white morph. Song frequency was unrelated to fitness, body size, or morph, but was individual specific and could signal individual identity. Songs of the two morphs displayed similar frequency ratios and bandwidths. However, tan morph males sang songs with longer first notes, fewer notes, and higher variability. Thus, song could be used in morph discrimination. Variation in frequency ratios between notes was low and could function in conspecific recognition, but pitch change dynamics did differ between four different song types observed. Our results support a multiple messages model for white‐throated sparrow song, in which different song traits communicate discrete information about the vocalizing individual.     

Reproductive phenology of the Azorean rock pool blenny a fish with alternative mating tactics

Both male and female Parablennius sanguinolentus parvicornis were ready to mate by the end of May. Seventy-five per cent of the 1-year-old males were mature, but only 25% of the females reached maturity at this age. In females, gonads formed an increasingly greater proportion of the total weight with age, but in males the proportion decreased. A bimodal distribution of gonadosomatic indices classes was observed in 2-year-old males (intermediate size), which reflected the lower opportunity that intermediate size males have to spend the ejaculates than have the younger and older males. The liver played an important role in the storage of energy before the reproductive season and reserves were utilized during the breeding season. Physical condition was at its lowest in July in both sexes, but in May, just before the breeding season began, large maturing females had significantly lower eviscerated condition than males. This could be due to females investing in oocyte development, while the priority for the males was to reserve their energy for the parental activities to come. In both males and females, older and bigger animals had lower hepatosomatic and body conditions than younger ones.     

Growth or reproduction: Intrasexual competition in a colonial damselfishStegastes nigricans

Intrasexual competition within colonies of the damselfishStegastes nigricans was investigated. Both males and females held individual territories, and these territories were adjacently distributed, forming distinct conspecific colonies with different size compositions. In both large and small colonies, only relatively large individuals participated in reproduction. Breeding males and females left their territories to court, spawn and aggregate more frequently than non-breeders of the same colonies. Breeders were less frequently attacked by other fish during these excursions than were non-breeders. Most attacks were conducted by breeders of the same sex. This intrasexual aggression may suppress the reproduction of non-breeders at least in large colonies. Non-breeders in large colonies had smaller gonads than breeders of both large and small colonies, but they grew faster than breeders of the same body size in small colonies. This suggests that non-breeders in large colonies allocate energy to growth in order to be reproductively competitive in the future, although only a few of them remained in the same colonies upon maturity. Colony size thus has an effect on the reproductive life histories of individual damselfish.     

Trade‐offs in female signal apparency to males offer alternative anti‐harassment strategies for colour polymorphic females

Colour polymorphisms are known to influence receiver behaviour, but how they affect a receiver's ability to detect and recognize individuals in nature is usually unknown. I hypothesized that polymorphic female damselflies represent an evolutionary stable strategy, maintained by trade‐offs between the relative apparency of morphs to male receivers. Using field experiments on Enallagma hageni and focal studies of E. hageni and Enallagma boreale, I tested for the first time the predictions that (i) green heteromorphs and blue andromorphs gain differential protection from sexual harassment via background crypsis and sexual mimicry, respectively, and (ii) female morphs behaviourally optimize their signal apparency to mate‐searching males. First, based on male reactions elicited by females, against a high‐contrast background, the two morphs did not differ in being detected by males, and once detected, they did not differ in being recognized (eliciting sexual reactions). However, on green ferns, heteromorphs were less likely to be detected (elicited only fly‐bys) than andromorphs, but once detected, the morphs did not differ in being recognized. In contrast, when perched on a dowel with two male signal distractors, andromorphs were detected less often, and once detected, they were recognized less often than heteromorphs. Second, in fields where females foraged, andromorphs perched higher on vegetation than heteromorphs and were more often in the vicinity of males. Neither harassment rates nor evasive behaviours differed between morphs. Males aggregated in high density near shore where solitary females were rare. Equilibrium frequencies of these and other colour morphs should reflect the relative ease with which receivers detect and recognize them in the context where they are encountered.     

The resident's dilemma: a female choice model for the evolution of alternative mating strategies in lekking male ruffs (Philomachus pugnax)

Previous models for the evolution of alternative male matingbehavior have virtually ignored the role of female choice. Wepresent a model in which female choice favors the evolutionand maintenance of alternative mating strategies in male ruffs,Philomachus pugnax. Resident male ruffe establish and defendcourts on leks against other residents, while non-territorialsatellite males move between leks and among courts on a lek.Residents appear to actively recruit satellites to their courts,even though satellites may mate with females once there. Residentbehavior toward satellites and data on female behavior suggestthat residents benefit from a satellite's presence due to somefemale preference for mating on co-occupied courts. However,if all residents accept satellites, none gains any relativeadvantage, yet all pay the costs of having satellites on theircourt. We present a game theoretical model that shows that therelative nature of female choice places residents in an evolutionarydilemma with respect to satellite acceptance. Although all residentswould benefit if satellites could be cooperatively excludedfrom leks, the only evolutionarily stable strategy for individualresidents is to defect and accept satellites. The model alsodemonstrates that this "resident's dilemma" likely exists onlyin a local sense, since the failure of residents to cooperativelyexclude satellites from leks need not result in globally lowerpayoffs, due to frequency-dependent selection on the proportionof satellites in the population. Our analysis suggests thatthe resident-satellite relationship in ruffs, despite its obviouscompetitive elements, is fundamentally a cooperative associationfavored by female choice. Female choice has also been proposedas the primary mechanism selecting for male association to formleks in ruffe. In this context, resident-satellite associationsmay be thought of as transitory "leks within a lek     

Evolution of alternative mating tactics: conditional versus mixed strategies

Intrasexual polymorphisms have evolved in a wide range of organisms.Most of them have been interpreted as the product of conditionalstrategies in which the tactic an individual adopts is determinedby some aspect of state (e.g., age, size, condition). However,there are a few examples that appear to represent an evolutionarilystable mixture of heritable pure strategies that are maintainedby frequency-dependent selection. In the present study, we producea model of a mating system with two morphs: a territorial morphand a sneak morph. By varying the costs and limits associatedwith conditional strategies, mating skew, and the proportionof matings obtained by sneaking males, we examine the conditionsthat favor the evolution of conditional versus pure strategies.Contrary to current thinking, our results show that as longas either costs or limits are greater than zero, conditionalstrategists are never able to entirely replace pure strategists,and equilibrium populations may frequently consist of a mixtureof conditional and pure strategists. Our results suggest thatconditional strategists will be most frequent at intermediatelevels of mating skew. Polymorphisms in which conditional strategistsare rare or absent are most likely to evolve when mating skewis extremely high, the costs and limits of plasticity are veryhigh, or the benefits of being conditional are very low. Thelimited data available suggest that high mating skew is probablythe most important factor.     

Intrasexual selection favours an immune‐correlated colour ornament in a dragonfly

Sexual signalling is predicted to shape the evolution of sex‐specific ornamentation, and establishing the costs and benefits of ornamentation and the information that ornamentation provides to receivers is necessary to evaluating this adaptive function. Here, we assessed the adaptive function of a common colour ornament in insects, melanin wing ornamentation, using the dragonfly Pachydiplax longipennis. We hypothesized that greater ornamentation would improve territory‐holding success by decreasing aggression that males receive from territorial rivals, but that more ornamented males may have shorter lifespans. Using mark–recapture field observations, we found that more ornamented males had greater territory‐holding success and that viability selection did not act on wing melanization. We then compared the aggression of territorial rivals to decoy males before and after experimentally augmenting wing melanization, finding that males significantly reduced aggression following the manipulation. We next hypothesized that wing melanization would signal fighting ability to territorial rivals by reflecting condition via investment in the costly melanin synthesis pathway. We observed a positive relationship between ornamentation and the likelihood of winning territorial disputes, suggesting that wing melanization provides information about fighting ability to rivals. We also found a positive relationship between melanin‐based immune defence and ornamentation, supporting a link between the signal and condition. We conclude that wing melanization is a condition‐related signal of fighting ability and suggest that this may be a common mechanism promoting the evolution of melanin ornamentation.     

Crypsis in a heterogeneous environment: relationships between changeable polymorphic colour patterns and behaviour in a galaxiid fish

1. The ability to achieve optimal camouflage varies between microhabitats in heterogeneous environments, potentially restricting individuals to a single habitat or imposing a compromise on crypsis to match several habitats. However, animals may exhibit morphological and behavioural attributes that enhance crypsis in different habitats. 2. We used an undescribed fish species, Galaxias‘nebula’, to investigate two objectives. First, we examined two potential methods of enhancing crypsis: change in colour pattern and selection of a suitable background. Second, we characterised the colour pattern of this unstudied fish and assessed its capacity for crypsis. 3. No background selection was apparent but the area of dark pigment expressed varied between backgrounds, which may negate the requirement to be choosy about habitats. The capacity to change colour and selection of a background that maximises crypsis are most likely separate, non‐mutually exclusive strategies. 4. Galaxias‘nebula’ exhibits polymorphic, non‐interchangeable colour patterns that have elements of both background pattern matching and disruptive colouration. This, coupled with habitat characteristics, suggests a combination of generalist and specialist strategies of habitat use. The fish’s camouflage strategy and air‐breathing ability may be key to survival under increasing pressure from habitat degradation and invasive predators.     

Forebrain arginine vasotocin correlates of alternative mating strategies in cricket frogs.

In cricket frogs, Acris crepitans, sexually active males can switch between calling and noncalling (satellite) mating strategies and injections of the neuropeptide arginine vasotocin (AVT) stimulate calling behavior. We report here that this behavioral variation of animals under field conditions is associated with variations in AVT-immunoreactive (AVT-ir) staining in distinct brain nuclei. In both calling and satellite males, one AVT-ir brain region was found in a continuous string of cells between the medial amygdala and the nucleus accumbens (ACC). Satellite males possessed significantly more AVT-ir staining in the brain (cells and fibers) than calling males at the level of the ACC, although not in the medial amygdala. This difference in AVT-ir staining in the ACC can, in part, be explained by differences in the density of staining within the cells and in cell size. In addition, satellite males had significantly higher AVT-ir staining in the fibers medial to the ACC than calling males. Because other studies have demonstrated that AVT stimulates calling behavior, a plausible hypothesis is that calling males are releasing more AVT from neurons in the ACC, depleting reserves within the cells, and that the released AVT elicits calling behavior. AVT immunoreactivity levels are also higher in the ACC in both calling and satellite males than in female cricket frogs, which do not call. Satellite males may therefore have AVT reserves that might allow them to call depending on the social conditions.