Habitat complexity drives experimental evolution of a conditionally expressed secondary sexual trait

The conditional expression of alternative phenotypes underlies the production of almost all life history decisions and many dichotomous traits, including male alternative reproductive morphs and behavioral tactics. Changes in tactic fitness should lead to evolutionary shifts in developmental switch points that underlie tactic expression. We used experimental evolution to directly test this hypothesis by rearing ten generations of the male-dimorphic mite Rhizoglyphus echinopus in either simple or three-dimensionally complex habitats that differed in their effects on morph fitness. In R. echinopus, fighter males develop weapons used for killing rivals, whereas scrambler males do not. Populations evolving in complex 3D habitats, where fighters had reduced fitness, produced fewer fighters because the switch point for fighter development evolved to a larger critical body size. Both the reduced mobility of fighter males and the altered spatial distribution of potential mates and rivals in the complex habitat were implicated in the evolutionary divergence of switch point between the habitats. Our results demonstrate how abiotic factors like habitat complexity can have a profound effect on evolution through sexual selection.     

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.     

The mechanisms of morph determination in the amphipod Jassa: implications for the evolution of alternative male phenotypes

The proximal basis for and the maintenance of alternative male reproductive strategies and tactics are generally not understood in most species, despite the occurrence of male polymorphism across many taxa. In the marine amphipod Jassa marmorata, males differ in morphology as well as behaviour. This dimorphism corresponds to two contrasting reproductive strategies: small sneaker males or 'minors', and large fighter males or 'majors'. This study uses quantitative genetic analyses in conjunction with experimental manipulations to assess the relative importance of genetic versus environmental factors in the determination and maintenance of these alternative mating strategies. Heritability analyses indicated the reproductive phenotypes do not reflect genetic differences between dimorphic males. By contrast, morph determination was significantly affected by diet quality. Majors essentially only developed on high-protein diets. Field studies also identified a strong correlation between seasonal shifts in the relative proportions of morphs and changes in food (i.e. phytoplankton) quantity and composition, corroborating that diet cues the switch between alternative reproductive tactics. Moreover, the comparison of major and minor growth trajectories identified a heterochronic shift in maturation times between morphs, indicating that ecological selective pressures, rather than just sexual selection, may be involved in the maintenance of this conditional strategy.     

Testing the status-dependent ESS model: population variation in fighter expression in the mite Sancassania berlesei

The conditional evolutionarily stable strategy (ESS) with status-dependent tactics is the most commonly invoked ESS for alternative reproductive tactics within the sexes. Support for this model has recently been criticized as apparent rather than real. We address key predictions of the status-dependent ESS in three populations of the male dimorphic mite Sancassania berlesei. In S. berlesei'fighter' males are characterized by a thickened pair of legs used for killing rivals; 'scramblers' are benign. Most males in each population could be manipulated to become fighters by decreasing density, fulfilling the prediction that males make a 'decision'. There was evidence of genetic covariance between sire status and offspring morph, but also a strong effect of sire morph on offspring morph ratio. This was consistent with considerable genetic variation for the status-dependent switch point as a breeding experiment found no support for single-locus inheritance. We also found evidence that switch points evolve independently of distributions of status. This study supports the current status-dependent ESS model.     

Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles

Sperm competition is widely recognized as a pervasive force of sexual selection. Theory predicts that across species increased risk of sperm competition should favor an increased expenditure on the ejaculate, a prediction for which there is much evidence. Sperm competition games have also been developed specifically for systems in which males adopt the alternative male mating tactics of sneaking copulations or guarding females. These models have not yet been tested in a comparative context, but predict that: across species male expenditure on the ejaculate should increase with increasing probability of a sneak mating; within species, sneaks should have the greater expenditure on the ejaculate; and the disparity in expenditure between sneaks and guards should be greatest in species with moderate risk of a sneak mating, and decline toward parity in species with low or high risk. Beetles in the genus Onthophagus are often characterized by dimorphic male morphologies that reflect the alternative mating tactics of sneak (minor males) and guard (major males). We conducted a comparative analysis across 16 species of male dimorphic onthophagines, finding that testes size increased across species with increasing frequency of the minor male phenotype. Minor males generally had the greater testes size, but across species the disparity between morphs was independent of the frequency of minor males. We present data on testes allometry from two populations of O. taurus that have undergone genetic divergence in the frequency of minor males. Consistent with the comparative analysis, these data support the notion that the relative frequency of sneaks in the population influences male expenditure on the ejaculate.     

Mixed evidence for the erosion of intertactical genetic correlations through intralocus tactical conflict

Alternative reproductive tactics, whereby members of the same sex use different tactics to secure matings, are often associated with conditional intrasexual dimorphisms. Given the different selective pressures on males adopting each mating tactic, intrasexual dimorphism is more likely to arise if phenotypes are genetically uncoupled and free to evolve towards their phenotypic optima. However, in this context, genetic correlations between male morphs could result in intralocus tactical conflict (ITC). We investigated the genetic architecture of male dimorphism in bulb mites (Rhizoglyphus echinopus) and earwigs (Forficula auricularia). We used half‐sibling breeding designs to assess the heritability and intra/intersexual genetic correlations of dimorphic and monomorphic traits in each species. We found two contrasting patterns; F. auricularia exhibited low intrasexual genetic correlations for the dimorphic trait, suggesting that the ITC is moving towards a resolution. Meanwhile, R. echinopus exhibited high and significant intrasexual genetic correlations for most traits, suggesting that morphs in the bulb mite may be limited in evolving to their optima. This also shows that intrasexual dimorphisms can evolve despite strong genetic constraints, contrary to current predictions. We discuss the implications of this genetic constraint and emphasize the potential importance of ITC for our understanding of intrasexual dimorphisms.     

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.     

Stress grows wings: environmental induction of winged dispersal males in Cardiocondyla ants

Dispersal is advantageous, but, at the same time, it implies high costs and risks. Due to these counteracting selection pressures, many species evolved dispersal polymorphisms, which, in ants, are typically restricted to the female sex (queens). Male polymorphism is presently only known from a few genera, such as Cardiocondyla, in which winged dispersing males coexist with wingless fighter males that mate exclusively inside their maternal nests. We studied the developmental mechanisms underlying these alternative male morphs and found that, first, male dimorphism is not genetically determined, but is induced by environmental conditions (decreasing temperature and density). Second, male morph is not yet fixed at the egg stage, but it differentiates during larval development. This flexible developmental pattern of male morphs allows Cardiocondyla ant colonies to react quickly to changes in their environment. Under good conditions, they invest exclusively in philopatric wingless males. But, when environmental conditions turn bad, colonies start to produce winged dispersal males, even though these males require a many times higher investment by the colony than their much smaller wingless counterparts. Cardiocondyla ants share this potential of optimal resource allocation with other colonial animals and some seed dimorphic plants.     

The adaptive significance of colour pattern polymorphism in the Australian scincid lizard Lampropholis delicata

Females of Lampropholis delicata are dimorphic for colour pattern, the difference between morphs being the presence or absence of a distinct white mid-lateral stripe. A less distinct striped morph occurs also in males. We evaluated alternative hypotheses for the maintenance of this polymorphism by examining temporal and spatial variation in morph frequency, testing for differential selection among morphs using data on body size and reproductive traits from preserved specimens, and experimentally manipulating colour pattern in free-ranging lizards of both sexes, to assess the influence of the lateral stripe on survival rates. We found that the relative frequency of striped individuals varied among populations and decreased from north to south in both sexes, coincident with an increasing incidence of regenerated tails. Morph frequencies did not change through time within a population. Striped gravid females appeared to survive better and produced larger clutches than did non-striped females. In our experimental study, the relationship between survival and colour morph differed between the two sexes; males painted with a white lateral stripe had lower survival than control (brown stripe) males, but survival did not differ between striped and control females. The different response in the two sexes may be due partly to differences in temperature and microhabitat selection. We propose that the white lateral stripe decreases susceptibility to predators in gravid females but increases risk of predation in males, especially in combination with low temperatures. The polymorphism might be maintained by: (1) opposing fitness consequences of the stripe in males and females; (2) sex-specific habitat selection; and (3) gene flow in combination with spatial variation in relative fitness of the two morphs.     

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.     

Age‐dependent male mating tactics in a spider mite—A life‐history perspective

Males often fight with rival males for access to females. However, some males display nonfighting tactics such as sneaking, satellite behavior, or female mimicking. When these mating tactics comprise a conditional strategy, they are often thought to be explained by resource holding potential (RHP), that is, nonfighting tactics are displayed by less competitive males who are more likely to lose a fight. The alternative mating tactics, however, can also be explained by life‐history theory, which predicts that young males avoid fighting, regardless of their RHP, if it pays off to wait for future reproduction. Here, we test whether the sneaking tactic displayed by young males of the two‐spotted spider mite can be explained by life‐history theory. We tested whether young sneaker males survive longer than young fighter males after a bout of mild or strong competition with old fighter males. We also investigated whether old males have a more protective outer skin—a possible proxy for RHP—by measuring cuticle hardness and elasticity using nanoindentation. We found that young sneaker males survived longer than young fighter males after mild male competition. This difference was not found after strong male competition, which suggests that induction of sneaking tactic is affected by male density. Hardness and elasticity of the skin did not vary with male age. Given that earlier work could also not detect morphometric differences between fighter and sneaker males, we conclude that there is no apparent increase in RHP with age in the mite and age‐dependent male mating tactics in the mite can be explained only by life‐history theory. Because it is likely that fighting incurs a survival cost, age‐dependent alternative mating tactics may be explained by life‐history theory in many species when reproduction of old males is a significant factor in fitness.     

Does frequency-dependence determine male morph survival in the bulb mite Rhizoglyphus robini?

Alternative reproductive phenotypes (ARPs) represent discrete morphological variation within a single sex; as such ARPs are an excellent study system to investigate the maintenance of phenotypic variation. ARPs are traditionally modelled as a mixture of pure strategies or as a conditional strategy. Most male dimorphisms are controlled by a conditional strategy, where males develop into a particular phenotype as a result of their condition which allows them to reach a certain threshold. Individuals that are unable to reach the threshold of a conditional strategy are considered to ‘make the best of a bad job’; however, these individuals can have their own fitness merits. Given these fitness merits, condition-dependent selection alone is not sufficient to maintain a conditionally determined male dimorphism and other mechanisms, most likely frequency-dependent selection, are required. We studied in an experiment, the male dimorphic bulb mite Rhizoglyphus robini—where males are fighters that can kill other males or benign scramblers—to assess the strength of frequency-dependent survival in a high and low-quality environment. We found that male survival was frequency-dependent in the high-quality environment but not the low-quality environment. In the high-quality environment the survival curves of the two morphs crossed but the direction of frequency-dependence was opposite to what theory predicts.     

Dimorphisms and fluctuating asymmetry in the forceps of male earwigs

Male dimorphisms are particularly conspicuous examples of the alternative reproductive strategies employed within some species. Such dimorphisms are thought to exist as genetic polymorphisms under ESS conditions, or to be conditional strategies where exogenous conditions determine the adult body plan. Fluctuating asymmetry (FA) is currently considered to be a fitness correlate of significant use in interpreting the functional significance of secondary sexual characteristics. In particular, negative slopes of FA on trait size are thought to arise in traits whose expression is dependent on condition. We measured forceps lengths and asymmetries in 2 island populations of the European earwig Forficula auricularia and Museum specimens of 5 other earwig (Dermaptera, Forficulidae) species from different genera, that appeared to be dimorphic. In a detailed study of Forficula auricularia we found a significant fit to a statistical model for the identification of dimorphisms and, for all species examined, morphs differed in the slope and/or elevation of the allometric relationship between body size and forcep length. Possible determinates of male dimorphisms are suggested from the data. Contrary to expectation, FA was not found to be greater in the minor morphs. Negative relationships between FA and forceps length were absent in both morphs of species examined from museum collections. Of the two island populations of Forficula auricularia, the smaller and more isolated population had higher FA and a negative relationship between FA and forceps length in the major morph. We discuss these patterns in the light of recent theories of FA and honest signalling.     

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.      

Status‐dependence and morphological trade‐offs in the expression of a sexually selected character in the mite,Sancassania berlesei

Abstract In the male dimorphic mite Sancassania berlesei, fighter males kill rivals with a pair of armoured legs whereas scrambler males are benign with unmodified legs. In an adaptive response mediated by colony pheromones, fighter expression increases at low colony density. Under the status‐dependent evolutionarily stable strategy (ESS) model we expected heavier final instar nymphs to become fighters. This was supported in group reared nymphs. In individually reared nymphs fighter expression was experimentally suppressed using two concentrations of colony pheromone. Here, male morph expression again depended on tritonymphal body mass and contact is therefore unnecessary for individuals to judge their status. Fighter suppression was greater in the higher pheromone treatment, but morph determination remained status dependent. The weight and length of fighters was lower than scramblers of same‐weight final instar nymphs, indicating a developmental trade‐off, and a cost not recouped at the adult stage.     

Effects of variation in nutrition on male morph development in the bulb mite Rhizoglyphus robini

In male dimorphic species, growth influences morph expression and thereby the reproductive success of males. However, how variation in nutritional conditions affects male morph development and whether males can compensate for lost growth is poorly known. Here, we performed an experiment where males of the bulb mite (Rhizoglyphus robini)—which are fighters, able to kill other mites, or benign scramblers—were offered high quality food during the larval stage, but food of high or low quality during the protonymph and tritonymph (=final) stage. When food quality was low during the latter two stages, males matured smaller, later and were more likely to be a scrambler than when food quality was high. We found no evidence for compensatory growth: when males had low quality food only during the protonymph stage, they matured at the same age, but grew at a slower rate and matured at a smaller size than males that had high quality food throughout ontogeny. Furthermore, males that experienced this transient period of low food quality were less likely to mature as a fighter. Interestingly, scrambler increase in body size during the protonymph and tritonymph stages was always lower than that of fighters. Given the strong link between adult size and fitness, combined with the different development times and life histories of the male morphs, the lack of ability to compensate for a transient period of food deprivation during ontogeny is likely to have consequences for the dynamics of bulb mite populations.     

Alternative Male Spawning Tactics and Acoustic Signals in the Plainfin Midshipman Fish Porichthys notatus Girard (Teleostei,Batrachoididae)

The plainfin midshipman Porichthys notatus has two male reproductive morphs, ‘Type I’ and ‘Type II’, which are distinguishable by their physical traits alone. Type I males are eight times larger in body mass than Type II males and have a six-fold larger relative sonic (vocal) muscle mass than Type II males. In contrast, the testicles of Type II males are seven times larger than those of Type I males. This study demonstrates morph-specific patterns of reproduction, including acoustic signals, for Type I and II males. Field censuses of nests showed that only Type 1 males maintained nests. Type II males and females transiently appeared in these nests in association with each other. Infra-red video and hydrophone recordings in aquaria showed that Type I males maintained nests and readily vocalized. Long-duration ‘hums’ and sequences of short-duration ‘grunts’ were produced during advertisement and agonistic contexts, respectively. Humming Type I males attracted females to their nests, pair-spawned, and then guarded egg clutches alone. By contrast, Type II males neither acoustically courted females nor maintained available nest sites, but rather ‘sneak-’ or ‘satellite-spawned’ at the nests of Type I males. Type II males infrequently produced low amplitude, short duration grunts that were similar in spectral, temporal and amplitude characteristics to the grunts of females. Type II males appear to be obligate sexual parasites of the nest-building, mate-calling, and egg-guarding Type I males. The dimorphic body and vocal muscle traits of the two male morphs in the plainfin midshipman are thus paralleled by a divergence in their reproductive tactics and the properties of their acoustic signals.     

Conditional male dimorphism and alternative reproductive tactics in a Neotropical arachnid (Opiliones)

In arthropods, most cases of morphological dimorphism within males are the result of a conditional evolutionarily stable strategy (ESS) with status-dependent tactics. In conditionally male-dimorphic species, the status’ distributions of male morphs often overlap, and the environmentally cued threshold model (ET) states that the degree of overlap depends on the genetic variation in the distribution of the switchpoints that determine which morph is expressed in each value of status. Here we describe male dimorphism and alternative mating behaviors in the harvestman Serracutisoma proximum. Majors express elongated second legs and use them in territorial fights; minors possess short second legs and do not fight, but rather sneak into majors’ territories and copulate with egg-guarding females. The static allometry of second legs reveals that major phenotype expression depends on body size (status), and that the switchpoint underlying the dimorphism presents a large amount of genetic variation in the population, which probably results from weak selective pressure on this trait. With a mark-recapture study, we show that major phenotype expression does not result in survival costs, which is consistent with our hypothesis that there is weak selection on the switchpoint. Finally, we demonstrate that switchpoint is independent of status distribution. In conclusion, our data support the ET model prediction that the genetic correlation between status and switchpoint is low, allowing the status distribution to evolve or to fluctuate seasonally, without any effect on the position of the mean switchpoint.     

Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite

Understanding the evolution and maintenance of within-sex reproductive morphs, or alternative reproductive phenotypes (ARPs), requires in depth understanding of the proximate mechanisms that determine ARP expression. Most species express ARPs in complex ecological environments, yet little is know about how different environmental variables collectively affect ARP expression. Here, I investigated the influence of maternal and developmental nutrition and sire phenotype on ARP expression in bulb mites (Rhizoglyphus robini), where males are either fighters, able to kill other mites, or benign scramblers. In a factorial experiment, females were raised on a rich or a poor diet, and after maturation they were paired to a fighter or a scrambler. Their offspring were put on the rich or poor diet. Females on the rich diet increased investment into eggs when mated to a fighter, but suffered reduced longevity. Females indirectly affected offspring ARP expression as larger eggs developed into larger final instars, which were more likely to develop into a fighter. Final instar size, which also strongly depended on offspring nutrition, was the main cue for morph development: a switch point, or size threshold, existed where development switched from one phenotype to the other. Sire phenotype affected offspring phenotype, but only if offspring were on the poor diet, indicating a gene by environment interaction. Overall, the results revealed that complex environmental effects can underlie ARP expression, with differential maternal investment potentially amplifying genetic effects on offspring morphology. These effects can therefore play an important role in understanding how selection affects ARP expression and, like quantitative genetics models for continuous traits, should be incorporated into models of threshold traits.