Stressful environments favor deceptive alternative mating tactics to become dominant.

BACKGROUND: Deceptive alternative mating tactics are commonly maintained at low frequencies within populations because males using them are less competitive and acquire lower fitness than those using dominant tactics. However, the successful invasion of a male deceptive tactic is plausible if deception carries no fitness cost to females. Among populations of the gift-giving spider Paratrechalea ornata, males very often offer females a deceptive worthless gift, rather than a nutritive gift. We tested the degree to which deceptive worthless gifts can occur in natural populations living under divergent environmental conditions (moderate and stressful). We examined the plasticity of morphological and behavioral traits and analyzed the fitness of females in relation to the gift type, also examining the paternity acquired by males offering either gift type. RESULTS: We demonstrated that worthless gifts can become dominant under highly stressful environmental conditions (84-100%). Individuals in such environment reach smaller sizes than those in moderate conditions. We suggest that the size reduction probably favors low metabolic demands in both sexes and may reduce the costs associated with receiving deceptive worthless gifts for females. In contrast, males living under moderate conditions varied the use of the deceptive tactic (0-95%), and worthless gifts negatively influenced female fecundity. Furthermore, male size, rather than gift content, positively impacted paternity success in the moderate but not in the stressful environment. CONCLUSIONS: Overall, this is the first empirical evidence that a reversible deceptive tactic can become dominant when the environment becomes harsh and mate choice becomes limited.

AnimalTraits - a curated animal trait database for body mass, metabolic rate and brain size.

Trait databases have become important resources for large-scale comparative studies in ecology and evolution. Here we introduce the AnimalTraits database, a curated database of body mass, metabolic rate and brain size, in standardised units, for terrestrial animals. The database has broad taxonomic breadth, including tetrapods, arthropods, molluscs and annelids from almost 2000 species and 1000 genera. All data recorded in the database are sourced from their original empirical publication, and the original metrics and measurements are included with each record. This allows for subsequent data transformations as required. We have included rich metadata to allow users to filter the dataset. The additional R scripts we provide will assist researchers with aggregating standardised observations into species-level trait values. Our goals are to provide this resource without restrictions, to keep the AnimalTraits database current, and to grow the number of relevant traits in the future.

The spatial and temporal distribution of females influence the evolution of testes size in Australian rodents.

Male-male competition after mating (sperm competition) favours adaptations in male traits, such as elevated sperm numbers facilitated by larger testes. Ultimately, patterns of female distribution will affect the strength of sperm competition by dictating the extent to which males are able to prevent female remating. Despite this, our understanding of how the spatial and temporal distributions of mating opportunities have shaped the evolutionary course of sperm competition is limited. Here, we use phylogenetic comparative methods to explore interspecific variation in testes size in relation to patterns of female distribution in Australian rodents. We find that as mating season length (temporal distribution of females) increases, testes size decreases, which is consistent with the idea that it is difficult for males to prevent females from remating when overlap among oestrous females is temporally concentrated. Additionally, we find that social species (spatially clustered) have smaller testes than non-social species (spatially dispersed). This result suggests that males may be effective in monopolizing reproduction within social groups, which leads to reduced levels of sperm competition relative to non-social species where free-ranging females cannot be controlled. Overall, our results show that patterns of female distribution, in both space and time, can influence the strength of post-mating sexual selection among species.

The first true millipede-1306 legs long.

The name "millipede" translates to a thousand feet (from mille "thousand" and pes "foot"). However, no millipede has ever been described with more than 750 legs. We discovered a new record-setting species of millipede with 1,306 legs, Eumillipes persephone, from Western Australia. This diminutive animal (0.95 mm wide, 95.7 mm long) has 330 segments, a cone-shaped head with enormous antennae, and a beak for feeding. A distant relative of the previous record holder, Illacme plenipes from California, it belongs to a different order, the Polyzoniida. Discovered 60 m below ground in a drill hole created for mineral exploration, E. persephone possesses troglomorphic features; it lacks eyes and pigmentation, and it has a greatly elongated body-features that stand in stark contrast to its closest surface-dwelling relatives in Australia and all other members of its order. Using phylogenomics, we found that super-elongation (> 180 segments) evolved repeatedly in the millipede class Diplopoda. The striking morphological similarity between E. persephone and I. plenipes is a result of convergent evolution, probably for locomotion in similar soil habitats. Discovered in the resource-rich Goldfields-Esperance region and threatened by encroaching surface mining, documentation of this species and conservation of its habitat are of critical importance.

Kin-mediated plasticity in alternative reproductive tactics.

Conditional strategies occur when the relative fitness pay-off from expressing a given phenotype is contingent upon environmental circumstances. This conditional strategy model underlies cases of alternative reproductive tactics, in which individuals of one sex employ different means to obtain reproduction. How kin structure affects the expression of alternative reproductive tactics remains unexplored. We address this using the mite Rhizoglyphus echinopus, in which large males develop into aggressive 'fighters' and small males develop into non-aggressive 'scramblers.' Because only fighters kill their rivals, they should incur a greater indirect fitness cost when competing with their relatives, and thus fighter expression could be reduced in the presence of relatives. We raised mites in full-sibling or mixed-sibship groups and found that fighters were more common at higher body weights in full-sibling groups, not less common as we predicted (small individuals were almost exclusively scramblers in both treatments). This result could be explained if relatedness and cue variability are interpreted signals of population density, since fighters are more common at low densities in this species. Alternatively, our results may indicate that males compete more intensely with relatives in this species. We provide the first evidence of kin-mediated plasticity in the expression of alternative reproductive tactics.

It is not always about body size: evidence of Rensch's rule in a male weapon.

In many species, sexual dimorphism increases with body size when males are the larger sex but decreases when females are the larger sex, a macro-evolutionary pattern known as Rensch's rule (RR). Although empirical studies usually focus exclusively on body size, Rensch's original proposal included sexual differences in other traits, such as ornaments and weapons. Here, we used a clade of harvestmen to investigate whether two traits follow RR: body size and length of the fourth pair of legs (legs IV), which are used as weapons in male-male fights. We found that males were slightly smaller than females and body size did not follow RR, whereas legs IV were much longer in males and followed RR. We propose that sexual selection might be stronger on legs IV length than on body size in males, and we discuss the potential role of condition dependence in the emergence of RR.

Trapped indoors? Long-distance dispersal in mygalomorph spiders and its effect on species ranges.

The Mygalomorphae includes tarantulas, trapdoor, funnel-web, purse-web and sheet-web spiders, species known for poor dispersal abilities. Here, we attempted to compile all the information available on their long-distance dispersal mechanisms from observations that are often spread throughout the taxonomic literature. Mygalomorphs can disperse terrestrially, and in some tarantulas, for example, spiderlings walk together in single files away from their maternal burrow, a mechanism limited in distance covered. Conversely, at least eight species disperse aerially, via dropping on drag lines from elevated positions and being passively blown off ('suspended ballooning'). The first record of this behaviour is 135 years old, but we still know very little about it. Phylogeographic studies suggest several occurrences of transcontinental dispersal in the evolutionary history of mygalomorphs, but these might result from contingent rafting events, rather than regular dispersal mechanisms. We use occurrence data to show that suspended ballooning increases the species ranges in Australian mygalomorph families where this behaviour has been recorded. We also identified Anamidae, Idiopidae, and especially Atracidae, as families that might employ suspended ballooning or another efficient but undiscovered dispersal mechanism. Finally, we suggest that molecular studies with mitochondrial genes will help disentangle behavioural limitations of dispersal from ecological or physical ones.

Selection for Male Weapons Boosts Female Fecundity, Eliminating Sexual Conflict in the Bulb Mite.

Extreme differences between the sexes are usually explained by intense sexual selection on male weapons or ornaments. Sexually antagonistic genes, with a positive effect on male traits but a negative effect on female fitness, create a negative inter-sexual correlation for fitness (sexual conflict). However, such antagonism might not be apparent if sexually selected male traits are condition-dependent, and condition elevates female fitness. Here we reveal a surprising positive genetic correlation between male weaponry and female fecundity. Using mite lines that had previously been through 13 generations of selection on male weapons (fighting legs), we investigated correlated evolution in female fecundity. Females from lines under positive selection for weapons (up lines) evolved higher fecundity, despite evolving costly, thicker legs. This is likely because male mites have condition-dependent weaponry that increases our ability to indirectly select on male condition. Alleles with positive effects on condition in both sexes could have generated this correlation because: the up lines evolved a higher proportion of fighters and there were positive correlations between weapon size and the male morph and sex ratios of the offspring. This positive inter-sexual genetic correlation should boost the evolution of male weapons and extreme sex differences.

Extreme and Variable Climatic Conditions Drive the Evolution of Sociality in Australian Rodents.

Climate change is generating an intensification of extreme environmental conditions, including frequent and severe droughts [1] that have been associated with increased social conflict in vertebrates [2-4], including humans [5]. Yet, fluctuating climatic conditions have been shown to also promote cooperative behavior and the formation of vertebrate societies over both ecological and evolutionary timescales [6]. Determining when climatic uncertainty breeds social discord or promotes cooperative living (or both) is fundamental to predicting how species will respond to anthropogenic climate change. In light of this, our limited understanding of the order of evolutionary events-that is, whether harsh environments drive the evolution of sociality [6] or, alternatively, whether sociality facilitates the invasion of harsh environments [7]-and of how cooperation and conflict coevolve in response to environmental fluctuation represent critical gaps in knowledge. Here, we perform comparative phylogenetic analyses on Australian rodents (Muridae: Hydromyini) and show that sociality evolves only under harsh conditions of low rainfall and high temperature variability and never under relatively benign conditions. Further, we demonstrate that the requirement to cooperate under harsh climatic conditions generates social competition for reproduction within groups (reflected in the degree of sexual dimorphism in traits associated with intrasexual competition [8]), which in turn shapes the evolution of body size dimorphism. Our findings suggest that as the environment becomes more severe [1], the resilience of some species may hinge on their propensity to live socially, but in so doing, this is likely to affect the evolution of traits that mediate social conflict.

Morph-specific artificial selection reveals a constraint on the evolution of polyphenisms.

Theory predicts that the evolution of polyphenic variation is facilitated where morphs are genetically uncoupled and free to evolve towards their phenotypic optima. However, the assumption that developmentally plastic morphs can evolve independently has not been tested directly. Using morph-specific artificial selection, we investigated correlated evolution between the sexes and male morphs of the bulb mite Rhizoglyphus echinopus Large 'fighter' males have a thick and sharply terminating pair of legs used to kill rival males, while small 'scrambler' males have unmodified legs, and search for unguarded females, avoiding fights. We selected on the relative leg width of only the fighter male morph, tracked the evolutionary responses in fighters and the correlated evolutionary responses in scramblers and females that were untouched by direct selection. Fighters diverged in relative leg thickness after six generations; assaying scramblers and females at the ninth generation we observed correlated responses in relative leg width in both. Our results represent strong evidence for the evolution of intraspecific phenotypic diversity despite correlated evolution between morphs and sexes, challenging the idea that male morphs are genetically uncoupled and free to independently respond to selection. We therefore question the perceived necessity for genetic independence in traits with extreme phenotypic plasticity.

Population density mediates the interaction between pre- and postmating sexual selection.

When females mate with more than one male, sexual selection acts both before and after mating. The interaction between pre- and postmating episodes of selection is expected to be context dependent, but few studies have investigated how total sexual selection changes under different ecological conditions. We examined how population density mediates the interaction between pre- and postmating sexual selection by establishing replicate populations of the horned dung beetle Onthophagus taurus at low, medium, and high densities, and then using microsatellite-based parentage analyses to measure male fitness. We found that mating success and fertilization success were positively correlated at all three densities, but the strength of the correlation decreased with increasing density. We also found a shift from negative to positive linear selection on testes mass as density increased, and opposing selection on weapons and testes at high densities. These patterns suggest that the importance of postmating processes increases with increasing population density, which reduces the selective advantage of weapons for premating contest competition, and increases the selective advantage of large ejaculates for postmating sperm competition. We expect that density-dependent selection on testes mass has contributed to the phenotypic variation observed between natural populations of O. taurus that differ in density.

Benefits of polyandry: Molecular evidence from field-caught dung beetles.

When females mate with multiple males, they set the stage for postcopulatory sexual selection via sperm competition and/or cryptic female choice. Surprisingly little is known about the rates of multiple mating by females in the wild, despite the importance of this information in understanding the potential for postcopulatory sexual selection to drive the evolution of reproductive behaviour, morphology and physiology. Dung beetles in the genus Onthophagus have become a laboratory model for studying pre- and postcopulatory sexual selection, yet we still lack information about the reproductive behaviour of female dung beetles in natural populations. Here, we develop microsatellite markers for Onthophagus taurus and use them to genotype the offspring of wild-caught females and to estimate natural rates of multiple mating and patterns of sperm utilization. We found that O. taurus females are highly polyandrous: 88% of females produced clutches sired by at least two males, and 5% produced clutches with as many as five sires. Several females (23%) produced clutches with significant paternity skew, indicating the potential for strong postcopulatory sexual selection in natural populations. There were also strong positive correlations between the number of offspring produced and both number of fathers and paternity skew, which suggests that females benefit from mating polyandrously by inciting postcopulatory mechanisms that bias paternity towards males that can sire more viable offspring. This study evaluates the fitness consequences of polyandry for an insect in the wild and provides strong evidence that female dung beetles benefit from multiple mating under natural conditions.

A model for conditional male trimorphisms.

Conditional dimorphisms are widespread in color, morphology, behavior, and life history. Such traits have been successfully modeled in game theory as conditional strategies, and in quantitative genetics as threshold traits. Conditional trimorphisms have recently been unveiled, and here we combine the rock-paper-scissors (RPS) model of game theory and the environmental threshold (ET) model of quantitative genetics to model trimorphisms that are environmentally induced and result from the expression of two thresholds. We investigated the tactic fitness structure for maintenance of alternative reproductive tactics in scarab dung beetles that constitute the first known examples of conditional male trimorphism. We parameterized a novel ternary fitness landscape that explains how conditional male trimorphism in these beetles can be maintained. We tracked changes in tactic frequencies in a wild population of Phanaeus triangularis and detected fitness intransitivity consistent with RPS dynamics. Quantitative predictions of our model compare favorably with corresponding observed parameters. The ternary landscape further reveals how geographic populations of these beetles can evolve between conditional trimorphism and dimorphism. The ternary model also suggests that polyphenic systems could potentially evolve between conditional and purely genetic mediation.

Sperm competition and the evolution of precopulatory weapons: Testis size and amplexus position, but not arm strength, affect fertilization success in a chorusing frog.

Trade-offs between pre- and postcopulatory traits influence their evolution, and male expenditure on such traits is predicted to depend on the number of competitors, the benefits from investing in weapons, and the risk and intensity of sperm competition. Males of the chorusing frog Crinia georgiana use their arms as weapons in contest competition. Previously, we showed that increased numbers of rivals elevated the risk and intensity of sperm competition due to multimale amplexus, and caused a reversal in the direction of precopulatory selection on arm girth. Here, we focused on the factors affecting postcopulatory fertilization success during group spawning, using paternity data from natural choruses. Competitive fertilization success depended on the time spent amplexed and amplexus position. Relative testes size but not arm girth, contributed to fertilization success, but the effect of testes size depended on amplexus position. Our findings offer within species empirical support for recent sperm competition models that incorporate precopulatory male-male competition, and show why an understanding of the evolution of animal weapons requires a consideration of both pre- and postcopulatory episodes of sexual selection.

Macroecology of Sexual Selection: A Predictive Conceptual Framework for Large-Scale Variation in Reproductive Traits.

Abiotic factors exert direct and indirect influences on behavioral, morphological, and life-history traits. Because some of these traits are related to reproduction, there is a causal link between climatic conditions and the expression of reproductive traits. This link allows us to generate predictions on how reproductive traits vary in large geographic scales. Here we formalize this macroecological framework, present some general predictions, and explore empirical examples using harvestmen as study organisms. Our results show that the length of breeding season in harvestmen is primarily influenced by the number of warm months and that precipitation plays a secondary role in modulating the period devoted to reproduction. Moreover, we show that the probability of resource defense polygyny increases with longer breeding seasons and that the presence of this type of mating system positively affects the magnitude of sexual dimorphism in harvestmen. Finally, the presence of postovipositional parental care is also influenced by the length of breeding season but not by actual evapotranspiration, which is our proxy for the intensity of biotic interactions. We argue that the macroecological framework proposed here may be a fruitful field of investigation, with important implications for our understanding of sexual selection and the evolution of reproductive traits in both animals and plants.

Investigating the genetic architecture of conditional strategies using the environmental threshold model.

The threshold expression of dichotomous phenotypes that are environmentally cued or induced comprise the vast majority of phenotypic dimorphisms in colour, morphology, behaviour and life history. Modelled as conditional strategies under the framework of evolutionary game theory, the quantitative genetic basis of these traits is a challenge to estimate. The challenge exists firstly because the phenotypic expression of the trait is dichotomous and secondly because the apparent environmental cue is separate from the biological signal pathway that induces the switch between phenotypes. It is the cryptic variation underlying the translation of cue to phenotype that we address here. With a 'half-sib common environment' and a 'family-level split environment' experiment, we examine the environmental and genetic influences that underlie male dimorphism in the earwig Forficula auricularia. From the conceptual framework of the latent environmental threshold (LET) model, we use pedigree information to dissect the genetic architecture of the threshold expression of forceps length. We investigate for the first time the strength of the correlation between observable and cryptic 'proximate' cues. Furthermore, in support of the environmental threshold model, we found no evidence for a genetic correlation between cue and the threshold between phenotypes. Our results show strong correlations between observable and proximate cues and less genetic variation for thresholds than previous studies have suggested. We discuss the importance of generating better estimates of the genetic variation for thresholds when investigating the genetic architecture and heritability of threshold traits. By investigating genetic architecture by means of the LET model, our study supports several key evolutionary ideas related to conditional strategies and improves our understanding of environmentally cued decisions.

Sperm competition and the evolution of precopulatory weapons: Increasing male density promotes sperm competition and reduces selection on arm strength in a chorusing frog.

Sperm competition theory assumes a trade-off between precopulatory traits that increase mating success and postcopulatory traits that increase fertilization success. Predictions for how sperm competition might affect male expenditure on these traits depend on the number of competing males, the advantage gained from expenditure on weapons, and the level of sperm competition. However, empirical tests of sperm competition theory rarely examine precopulatory male expenditure. We investigated how variation in male density affects precopulatory sexual selection on male weaponry and the level of sperm competition in the chorusing frog Crinia georgiana, where males use their arms as weapons in male-male combat. We measured body size and arm girth of 439 males, and recorded their mating success in the field. We found density-dependent selection acting on arm girth. Arm girth was positively associated with mating success, but only at low population densities. Increased male density was associated with higher risk and intensity of sperm competition arising from multimale amplexus, and a reversal in the direction of selection on arm girth. Opposing patterns of pre- and postcopulatory selection may account for the negative covariation between arm girth and testes across populations of this species.

Male dimorphism and alternative reproductive tactics in harvestmen (Arachnida: Opiliones).

Strong sexual selection may lead small males or males in poor condition to adopt alternative reproductive tactics (ARTs) as a way to avoid the risk of being completely excluded from the mating pool. ARTs, sometimes accompanying morphological dimorphism among males, are taxonomically widespread, especially common in arthropods. Here we review the current knowledge on ARTs and male dimorphism in a diverse but relatively overlooked group of arachnids, the order Opiliones, popularly known as harvestmen or daddy long-legs. We begin with a summary of harvestman mating systems, followed by a review of the two lines of evidence for the presence of ARTs in the group: (1) morphological data from natural populations and museum collections; and (2) behavioral information from field studies. Despite receiving less attention than spiders, scorpions and insects, our review shows that harvestmen are an exciting group of organisms that are potentially great models for sexual selection studies focused on ARTs. We also suggest that investigating the proximate mechanisms underlying male dimorphism in the order would be especially important. New research on ARTs and male dimorphism will have implications for our understanding of the evolution of mating systems, sperm competition, and polyandry. This article is part of a Special Issue entitled: Neotropical Behaviour.

Correlated evolution of sexual dimorphism and male dimorphism in a clade of neotropical harvestmen.

Secondary sexual traits increase male fitness, but may be maladaptive in females, generating intralocus sexual conflict that is ameliorated through sexual dimorphism. Sexual selection on males may also lead some males to avoid expenditure on secondary sexual traits and achieve copulations using alternative reproductive tactics (ARTs). Secondary sexual traits can increase or decrease fitness in males, depending on which ART they employ, generating intralocus tactical conflict that can be ameliorated through male dimorphism. Due to the evolutionary forces acting against intralocus sexual and tactical conflicts, male dimorphism could coevolve with sexual dimorphism, a hypothesis that we tested by investigating these dimorphisms across 48 harvestman species. Using three independently derived phylogenies, we consistently found that the evolution of sexual dimorphism was correlated with that of male dimorphism, and suggest that the major force behind this relationship is the similarity between selection against intralocus sexual conflict and selection against intralocus tactical conflict. We also found that transitions in male dimorphism were more likely in the presence of sexual dimorphism, indicating that if a sexually selected trait arises on an autosome and is expressed in both sexes, its suppression in females probably evolves earlier than its suppression in small males that adopt ARTs.