Juvenile leg autotomy predicts adult male morph in a New Zealand harvestman with weapon polymorphism.

Intraspecific weapon polymorphisms that arise via conditional thresholds may be affected by juvenile experience such as predator encounters, yet this idea has rarely been tested. The New Zealand harvestman Forsteropsalis pureora has three male morphs: majors (alphas and betas) are large-bodied with large chelicerae used in male-male contests, while minors (gammas) are small-bodied with small chelicerae and scramble to find mates. Individuals use leg autotomy to escape predators and there is no regeneration of the missing leg. Here, we tested whether juvenile experience affects adult morph using leg autotomy scars as a proxy of predator encounters. Juvenile males that lost at least one leg (with either locomotory or sensory function) had a 45 times higher probability of becoming a minor morph at adulthood than intact juvenile males. Leg loss during development may affect foraging, locomotion, and/or physiology, potentially linking a juvenile's predator encounters to their final adult morph and future reproductive tactic.

Camouflage in lichen moths: Field predation experiments and avian vision modelling demonstrate the importance of wing pattern elements and background for survival.

Background matching is perhaps the most ubiquitous form of defensive camouflage in the animal kingdom, an adaptive strategy that relies on the visual resemblance between a prey organism and its background to promote concealment from predators. The importance of background matching has been acknowledged for over a century, yet despite its renown and apparent pervasiveness, few studies exist that have objectively quantified its occurrence and tested the functional significance of background matching in a specific animal study system. The North Island lichen moth Declana atronivea presents a fascinating system to investigate such anti-predator coloration. This species possesses high contrast black and white forewings that appear to resemble lichen. Here we assessed the contribution of background matching to the antipredator defence of D. atronivea using field predation experiments with realistic models. We found that D. atronivea coloration confers a significant survival advantage against native avian predators when on lichen backgrounds compared to bark backgrounds, with an intermediate level of predation occurring when models were near, but not on lichen. This suggests that D. atronivea wing patterns are an adaptation for background matching. We subsequently used calibrated digital photography, avian vision modelling and image analysis techniques to objectively quantify the degree of background matching exhibited by D. atronivea and assessed the contribution of different visual elements (colour, luminance and pattern) to camouflage in this species. Only the pattern elements of D. atronivea presented a close match to that of the lichen backgrounds, with both chromatic and achromatic cues found to be poor predictors of background matching in this species. This study is one of the first to integrate vision modelling, quantitative image analysis and field predation experiments using realistic models to objectively quantify the level and functional significance of background matching in a real species, and presents an ideal system for further investigating the interrelation between multiple mechanisms of camouflage.

Male coercion and female injury in a sexually cannibalistic mantis.

Sexual conflict can generate coercive traits in males that enhance mating success at the expense of female fitness. Pre-copulatory sexual cannibalism-where females consume males without mating-typically favours cautious rather than coercive mating tactics, and few examples of the latter are known. Here, we show that males of the highly cannibalistic springbok mantis, Miomantis caffra, wrestle females during pre-mating interactions. We find that most initial contacts between males and females involve a violent struggle whereby each sex tries be the first to grasp hold of the other with their raptorial forelegs. When females win the struggle, they always cannibalize males. However, when males grasp females first, they dramatically increase the chance of mating. We also find striking evidence that, on some occasions, males wound females with their fore-tibial claws during struggles, resulting in haemolymph loss and scar tissue formation. Taken together, our results show how males can overcome the threat of cannibalism by coercively wrestling females. We argue that pre-copulatory injury in this species is likely to be a negative pleiotropic side-effect of coercive mating behaviour and foraging morphology.

Cybernetic combatants support the importance of duels in the evolution of extreme weapons.

A current evolutionary hypothesis predicts that the most extreme forms of animal weaponry arise in systems where combatants fight each other one-to-one, in duels. It has also been suggested that arms races in human interstate conflicts are more likely to escalate in cases where there are only two opponents. However, directly testing whether duels matter for weapon investment is difficult in animals and impossible in interstate conflicts. Here, we test whether superior combatants experience a disproportionate advantage in duels, as compared with multi-combatant skirmishes, in a system analogous to both animal and military contests: the battles fought by artificial intelligence agents in a computer war game. We found that combatants with experimentally improved fighting power had a large advantage in duels, but that this advantage deteriorated as the complexity of the battlefield was increased by the addition of further combatants. This pattern remained under the two different forms of the advantage granted to our focal artificial intelligence (AI) combatants, and became reversed when we switched the roles to feature a weak focal AI among strong opponents. Our results suggest that one-on-one combat may trigger arms races in diverse systems. These results corroborate the outcomes of studies of both animal and interstate contests, and suggest that elements of animal contest theory may be widely applicable to arms races generally.

Mate-finding Allee effects can be exacerbated or relieved by sexual cannibalism.

Allee effects occur when individual or population survival decreases due to populations being small or sparse. A key mechanism underlying Allee effects is difficulty in finding mates at low densities. Species may be particularly vulnerable to mate-finding Allee effects if females rely on an abundance of males to reproduce successfully. In sexually cannibalistic species, females may consume males before or after copulation, potentially reducing the supply of males to the point where a mate-finding Allee effect occurs. In this study, we investigate the extent to which sexual cannibalism can modulate mate-finding Allee effects, and the conditions under which sexual cannibalism is likely to be particularly detrimental to population viability. We created an individual-based model that tracked specific females throughout the breeding season and used extinction risk and per capita growth rate to measure the strength of the Allee effects. We varied both founder population size and mate encounter rate independently of each other to expose the mechanism driving the Allee effects. We also analysed how cannibalism-derived female fecundity benefits affected extinction risk. We found that sexual cannibalism could lead to high extinction risk, particularly when cannibalism occurred before copulation, founder population size was small and mate encounter rates were low. However, post-copulatory cannibalism reduced extinction risk, if cannibalism increased female fecundity enough. We found that there were strong threshold effects, in which small changes in encounter rate could strongly alter population extinction risk. We find that sexual cannibalism is likely to negatively impact population survival as population size and mate encounter rate decrease. This may be exacerbated if male quality declines and female hunger increases in declining populations. As many top invertebrate predators, such as spiders and mantises, are sexually cannibalistic, this may have ecosystem-wide impacts. We also suggest that other reproductive behaviours, such as rejecting all but high-quality mates or requiring multiple mates to ensure fertility, are also likely to cause mate-finding Allee effects when habitat quality degrades.

Muscle mass drives cost in sexually selected arthropod weapons.

Sexually selected weapons often function as honest signals of fighting ability. If poor-quality individuals produce high-quality weapons, then receivers should focus on other, more reliable signals. Cost is one way to maintain signal integrity. The costs of weapons tend to increase with relative weapon size, and thereby restrict large weapons to high-quality individuals who can produce and maintain them. Weapon cost, however, appears to be unpredictably variable both within and across taxa, and the mechanisms underlying this variation remain unclear. We suggest variation in weapon cost may result from variation in weapon composition-specifically, differences in the amount of muscle mass directly associated with the weapon. We test this idea by measuring the metabolic cost of sexually selected weapons in seven arthropod species and relating these measures to weapon muscle mass. We show that individuals with relatively large weapon muscles have disproportionately high resting metabolic rates and provide evidence that this trend is driven by weapon muscle mass. Overall, our results suggest that variation in weapon cost can be partially explained by variation in weapon morphology and that the integrity of weapon signals may be maintained by increased metabolic cost in species with relatively high weapon muscle mass.

Directional selection on body size but no apparent survival cost to being large in wild New Zealand giraffe weevils.

When an individual's reproductive success relies on winning fights to secure mating opportunities, bearing larger weapons is advantageous. However, sexual selection can be extremely complex, and over an animal's life the opportunity to mate is influenced by numerous factors. We studied a wild population of giraffe weevils (Lasiorhynchus barbicornis) that exhibit enormous intra and intersexual size variation. Males bear an elongated rostrum used as a weapon in fights for mating opportunities. However, small males also employ sneaking behavior as an alternative reproductive tactic. We investigated sexual selection on size by tracking individual males and females daily over two 30-day periods to measure long-term mating success. We also assessed how survival and recapture probabilities vary with sex and size to determine whether there might be a survival cost associated with size. We found evidence for directional selection on size through higher mating success, but no apparent survival trade-off. Instead, larger individuals mate more often and have a higher survival probability, suggesting an accumulation of benefits to bigger individuals. Furthermore, we found evidence of size assortative mating where males appear to selectively mate with bigger females. Larger and more competitive males secure matings with larger females more frequently than smaller males, which may further increase their fitness.

Weak premating isolation between Clitarchus stick insect species despite divergent male and female genital morphology.

Documenting natural hybrid systems builds our understanding of mate choice, reproductive isolation and speciation. The stick insect species Clitarchus hookeri and C. tepaki differ in their genital morphology and hybridize along a narrow peninsula in northern New Zealand. We utilize three lines of evidence to understand the role of premating isolation and species boundaries: (a) genetic differentiation using microsatellites and mitochondrial DNA; (b) variation in 3D surface topology of male claspers and 2D morphometrics of female opercular organs; and (c) behavioural reproductive isolation among parental and hybrid populations through mating crosses. The genetic data show introgression between the parental species and formation of a genetically variable hybrid swarm. Similarly, the male and female morphometric data show genital divergence between the parental species as well as increased variation within the hybrid populations. This genital divergence has not resulted in reproductive isolation between species, instead weak perimating isolation has enabled the formation of a hybrid swarm. Behavioural analysis demonstrates that the entire mating process influences the degree of reproductive isolation between species undergoing secondary contact. Mechanical isolation may appear strong, whereas perimating isolation is weak.

Sexual cannibalism and population viability.

Some behaviours that typically increase fitness at the individual level may reduce population persistence, particularly in the face of environmental changes. Sexual cannibalism is an extreme mating behaviour which typically involves a male being devoured by the female immediately before, during or after copulation, and is widespread amongst predatory invertebrates. Although the individual-level effects of sexual cannibalism are reasonably well understood, very little is known about the population-level effects. We constructed both a mathematical model and an individual-based model to predict how sexual cannibalism might affect population growth rate and extinction risk. We found that in the absence of any cannibalism-derived fecundity benefit, sexual cannibalism is always detrimental to population growth rate and leads to a higher population extinction risk. Increasing the fecundity benefits of sexual cannibalism leads to a consistently higher population growth rate and likely a lower extinction risk. However, even if cannibalism-derived fecundity benefits are large, very high rates of sexual cannibalism (>70%) can still drive the population to negative growth and potential extinction. Pre-copulatory cannibalism was particularly damaging for population growth rates and was the main predictor of growth declining below the replacement rate. Surprisingly, post-copulatory cannibalism had a largely positive effect on population growth rate when fecundity benefits were present. This study is the first to formally estimate the population-level effects of sexual cannibalism. We highlight the detrimental effect sexual cannibalism may have on population viability if (1) cannibalism rates become high, and/or (2) cannibalism-derived fecundity benefits become low. Decreased food availability could plausibly both increase the frequency of cannibalism, and reduce the fecundity benefit of cannibalism, suggesting that sexual cannibalism may increase the risk of population collapse in the face of environmental change.

Exaggerated male legs increase mating success by reducing disturbance to females in the cave weta Pachyrhamma waitomoensis.

Mate guarding is a widespread behaviour resulting from sperm competition and conflict over optimal remating rates. It is a key way in which males exhibit differential mating investment, and represents a complex interplay between mating effort, intrasexual competition, opportunity costs and sexual conflict. Nevertheless, although there are many examples of exaggerated male structures used to fight rivals, few animals have developed specialized male morphological adaptations for directly sheltering females from disturbance by non-rivals. Here we report on the use of sexually dimorphic, elongated male hind legs, which are used to guard females in the New Zealand cave weta Pachyrhamma waitomoensis (Orthoptera: Rhaphidophoridae). We found that male hind legs alongside the female failed to deter rivals from accessing her or disrupting copulation. However, they did reduce the disturbance to females from other, non-rival animals such as juveniles and heterospecifics. Males with longer hind legs were more effective in reducing disturbance, and remained with females for longer. Longer guarding periods also led to higher numbers of matings between pairs. Models of males with artificially altered hind leg dimensions also showed a benefit to greater leg length, and artificially altering the disturbance rate to females also had a significant effect on pair duration. Our results indicate that nuisance disturbance to females may play an important role in driving sexual selection on male leg length and its exaggeration in this species.

Geometric morphometrics and molecular systematics of Xanthocnemis sobrina (McLachlan, 1873) (Odonata: Coenagrionidae) and comparison to its congeners.

The taxonomy of the damselfly genus Xanthocnemis is revised, with particular focus on populations inhabiting the North Island of New Zealand. Earlier studies revealed two species: X. sobrina, restricted to cool, shaded streams in kauri forests and other forested areas, and X. zealandica, a common species throughout New Zealand except the Chatham and subantarctic islands. A field study encompassing aquatic habitats throughout the whole North Island was carried out to establish the relationship between morphological variation (body size and various morphological traits over the entire body) observed by previous researchers with ecological conditions and/or geographical location. The main aim was to propose reliable diagnostic features that could be used in future studies. Morphological and molecular variation was assessed. Morphological examination included assigning landmarks for all body parts corresponding to the external morphological features that are usually used in Odonata taxonomy. Molecular analysis targeted fragments of the 28S and 16S rRNA genes. Congruence was sought between both types of data, statistical support for two morphological types previously described as different species and a maximum likelihood phylogenetic tree in conjunction with a pairwise genetic distance matrix constructed from the DNA sequences obtained from the sampled specimens. Geometric morphometrics revealed statistically significant differentiation between specimens identified as X. zealandica and X. sobrina for four traits: (1) dorsal view of the head for both sexes as well as male appendages from (2) dorsal, (3) ventral and (4) lateral views. Wings appeared different when analysed for males only. Molecular analysis, however, grouped all specimens into a single undifferentiated cluster with very low mean pairwise distance (<0.01) between them showing almost no variation at the molecular level among the sampled populations on the North Island. Therefore, an additional analysis of the mitochondrial cytochrome c-oxidase I gene was carried out comparing randomly selected North Island specimens to Xanthocnemis specimens targeted in other molecular studies (Nolan et al. 2007, Amaya-Perilla et al. 2014). The analysis of the COI gene confirmed that all North and South Island isolates of Xanthocnemis cluster together in a well-supported clade with pairwise identity >96% and ~93% pairwise identity with X. tuanuii sequences obtained from the Chatham Island specimens. A careful investigation of the thin plate spline deformations generated for the geometric morphometric landmarks showed that the significant variations in the appendages of the Xanthocnemis specimens appeared to be the result of size, rather than shape, differences. Therefore, X. sobrina is proposed as a synonym of X. zealandica. Recently Amaya-Perilla et al. (2014) synonymised X. sinclairi with X. zealandica and confirmed the status of the Chatham Island X. tuanuii as a distinct species. It is therefore proposed that the genus Xanthocnemis consists of two species only: zealandica occurring all over the North, South and Stewart Islands, and tuanuii, endemic to Chatham and Pitt islands. Considering several statistical tests involving body measurements and ecological variables recorded during the field study, as well as various discussion points from similar studies of other species of Odonata, two alternative hypotheses are proposed for future testing. The first hypothesis synonymises X. sobrina with X. zealandica and suggests a possible explanation for the evolution of the two morphological traits that have previously been considered diagnostic for these species. The second hypothesis suggests that as typical X. sobrina were not sampled during this study this could represent a species that is now extinct, unless future studies prove it otherwise.

Multiple exaggerated weapon morphs: a novel form of male polymorphism in harvestmen.

Alternative reproductive tactics in animals are commonly associated with distinct male phenotypes resulting in polymorphism of sexually selected weapons such as horns and spines. Typically, morphs are divided between small (unarmed) and large (armed) males according to one or more developmental thresholds in association with body size. Here, we describe remarkable weapon trimorphism within a single species, where two exaggerated weapon morphs and a third morph with reduced weaponry are present. Male Pantopsalis cheliferoides harvestmen display exaggerated chelicerae (jaws) which are highly variable in length among individuals. Across the same body size spectrum, however, some males belong to a distinct second exaggerated morph which possesses short, broad chelicerae. Multiple weapon morphs in a single species is a previously unknown phenomenon and our findings have significant implications for understanding weapon diversity and maintenance of polymorphism. Specifically, this species will be a valuable model for testing how weapons diverge by being able to test directly for the circumstances under which a certain weapon type is favoured and how weapon shape relates to performance.

The Functional Significance of Chiral Genitalia: Patterns of Asymmetry, Functional Morphology and Mating Success in the Praying Mantis Ciulfina baldersoni.

Genital asymmetry is relatively common and widespread throughout the animal kingdom. The functional significance of genital asymmetry is however, poorly understood for most species. Male praying mantids of the genus Ciulfina are remarkable in possessing complex and directionally asymmetric genital phallomeres in some species, and chirally dimorphic/antisymmetric genitalia in others. Here we explore the chiral dimorphism in male genitalia of Ciulfina baldersoni which appear to exhibit genital antisymmetry. We test whether genital orientation influences mating success, copulation duration and the attachment duration of spermatophores. Additionally we investigate genital interactions between male and females using x-ray micro-computed tomography (micro-CT) and scanning electron microscopy (SEM). Lastly we assess whether genital asymmetry is associated with non-genital morphological asymmetry of a range of traits. Our results highlight the complex functional morphology of genitalia in this praying mantis species and yet demonstrate no functional difference between dextral and sinistral morphs other than the direction of attachment with both morphs enjoying equal levels of mating success. Chiral morphs also did not strongly associate with any other forms of asymmetry. We therefore conclude that genital chirality in Ciulfina baldersoni is a likely case of antisymmetry with no functional significance to genital orientation, and is likely to be selectively neutral.

Four new species of Ciulfina Giglio-Tos, 1915 (Mantodea: Liturgusidae, Liturgusinae) from the Northern Territory, Australia .

The praying mantid genus Ciulfina Giglio-Tos includes many small, gracile tree-trunk dwelling species found throughout northern Australia. Four new species of Ciulfina: C. annecharlotteae, C. herbersteinae, C. ianrichardi, and C. terrymariceae are formally described on the basis of male genital morphology.

Pollinator deception in the orchid mantis.

Mimicry has evolved in contexts such as camouflage, predator deterrence, luring of prey, and pollinator attraction. Mimicry of flowers has until now been demonstrated only in angiosperms, yet it has been hypothesized that the Malaysian orchid mantis Hymenopus coronatus mimics a flower to attract pollinators as prey. Despite the popularity of this charismatic insect, this long-discussed hypothesis has never been experimentally investigated. We found that, as predicted for mimicry, the color of H. coronatus is indistinguishable from the color of sympatric flowers for hymenopteran pollinators. Field experiments show that isolated mantises attract wild pollinators at a rate even higher than flowers and capture these pollinators as prey items. After more than a century of conjecture, we provide the first experimental evidence of pollinator deception in the orchid mantis and the first description of a unique predatory strategy that has not been documented in any other animal species.

Different paths to sexual size dimorphism in two praying mantids, Pseudomantis albofimbriata and Hierodula majuscula.

Sexual size dimorphism (SSD) is widespread among diverse animal taxa and has attracted the attention of evolutionary biologists for over a century. SSD is likely to be adaptive and the result of divergent selection on different size optima for males and females, given their different roles in reproduction. The developmental trajectory leading to SSD may help us to understand how selection acts on male and female size. Here, we describe the growth and development of two Australian praying mantids, Pseudomantis albofimbriata and Hierodula majuscula including the number of moults, time to adulthood, size at each moult, and the degree of SSD. While both species exhibit the common pattern of female-biased SSD, the number of moults required for individuals to reach adulthood differed between males and females and between species. Despite their larger adult size, P. albofimbriata females require fewer moults and less time than males to reach adulthood, but are significantly larger than males from the second instar onwards. In contrast, H. majuscula males reached adulthood in fewer moults, and less time than females, however males and females did not differ in size until females went through their final moult into adulthood. H. majuscula also required more time and more moults to reach adulthood than P. albofimbriata. We discuss these different developmental pathways in light of the existing knowledge of reproductive biology for each species. We also suggest that these differences may relate to the different phenologies that occur in strongly seasonal temperate environments compared with those in the tropics. This study provides evidence that SSD can result from two different patterns of growth and development in closely related species.

Exaggerated trait allometry, compensation and trade-offs in the New Zealand giraffe weevil (Lasiorhynchus barbicornis).

Sexual selection has driven the evolution of exaggerated traits among diverse animal taxa. The production of exaggerated traits can come at a cost to other traits through trade-offs when resources allocated to trait development are limited. Alternatively some traits can be selected for in parallel to support or compensate for the cost of bearing the exaggerated trait. Male giraffe weevils (Lasiorhynchus barbicornis) display an extremely elongated rostrum used as a weapon during contests for mates. Here we characterise the scaling relationship between rostrum and body size and show that males have a steep positive allometry, but that the slope is non-linear due to a relative reduction in rostrum length for the largest males, suggesting a limitation in resource allocation or a diminishing requirement for large males to invest increasingly into larger rostra. We also measured testes, wings, antennae, fore- and hind-tibia size and found no evidence of a trade-off between these traits and rostrum length when comparing phenotypic correlations. However, the relative length of wings, antennae, fore- and hind-tibia all increased with relative rostrum length suggesting these traits may be under correlational selection. Increased investment in wing and leg length is therefore likely to compensate for the costs of flying with, and wielding the exaggerated rostrum of larger male giraffe weevils. These results provide a first step in identifying the potential for trait compensation and trades-offs, but are phenotypic correlations only and should be interpreted with care in the absence of breeding experiments.

Fatal attraction: sexually cannibalistic invaders attract naive native mantids.

Overlap in the form of sexual signals such as pheromones raises the possibility of reproductive interference by invasive species on similar, yet naive native species. Here, we test the potential for reproductive interference through heterospecific mate attraction and subsequent predation of males by females of a sexually cannibalistic invasive praying mantis. Miomantis caffra is invasive in New Zealand, where it is widely considered to be displacing the only native mantis species, Orthodera novaezealandiae, and yet mechanisms behind this displacement are unknown. We demonstrate that native males are more attracted to the chemical cues of introduced females than those of conspecific females. Heterospecific pairings also resulted in a high degree of mortality for native males. This provides evidence for a mechanism behind displacement that has until now been undetected and highlights the potential for reproductive interference to greatly influence the impact of an invasive species.

Ferocious fighting between male grasshoppers.

Contests among individuals over mating opportunities are common across diverse taxa, yet physical conflict is relatively rare. Due to the potentially fatal consequences of physical fighting, most animals employ mechanisms of conflict resolution involving signalling and ritualistic assessment. Here we provide the first evidence of ubiquitous escalated fighting in grasshoppers. The chameleon grasshopper (Kosciuscola tristis) is an Australian alpine specialist, in which males engage in highly aggressive combat over ovipositing females. We describe discrete agonistic behaviours including mandible flaring, mounting, grappling, kicking and biting, and their use depending on the individual's role as challenger or defender. We show that male role predicts damage, with challengers being more heavily damaged than males defending females (defenders). Challengers also possess wider mandibles than defenders, but are similar in other metrics of body size. Our data suggest that fights escalate between males matched in body size and that mandibles are used as weapons in this species. This system represents an exciting opportunity for future research into the evolution of costly fighting behaviour in an otherwise placid group.

Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification.

The role of sexual selection in fuelling genital evolution is becoming increasingly apparent from comparative studies revealing interspecific divergence in male genitalia and evolutionary associations between male and female genital traits. Despite this, we know little about intraspecific variance in male genital morphology, or how male and female reproductive traits covary among divergent populations. Here we address both topics using natural populations of the guppy, Poecilia reticulata, a livebearing fish that exhibits divergent patterns of male sexual behaviour among populations. Initially, we performed a series of mating trials on a single population to examine the relationship between the morphology of the male's copulatory organ (the gonopodium) and the success of forced matings. Using a combination of linear measurements and geometric morphometrics, we found that variation in the length and shape of the gonopodium predicted the success of forced matings in terms of the rate of genital contacts and insemination success, respectively. We then looked for geographical divergence in these traits, since the relative frequency of forced matings tends to be greater in high-predation populations. We found consistent patterns of variation in male genital size and shape in relation to the level of predation, and corresponding patterns of (co)variation in female genital morphology. Together, these data enable us to draw tentative conclusions about the underlying selective pressures causing correlated patterns of divergence in male and female genital traits, which point to a role for sexually antagonistic selection.