Hemideina Crassidens Research Articles

Alternative mating strategies in the Wellington tree weta expressed via genetic polymorphism for precocial male maturation.

The expression of alternative mating strategies is generally hypothesized to be a plastic response of the genome to the environment or a genetic polymorphism. The Wellington tree weta (Hemideina crassidens) is an orthopteran insect in which males express three alternative mating morphotypes related to the size of mandibular weaponry. My common garden experiment in the laboratory shows that male weapon size at maturity in this species is nether condition- nor environment-dependent; therefore, supporting the hypothesis that it is genetically polymorphic. Males that matured at the 8th instar had the shortest development time and the smallest weaponry, males that matured at the 10th instar had the longest development time and the largest weaponry, and males that matured at the 9th instar were intermediate to the other two morphs. These morph-related differences in development time suggest that male alternative mating strategies in this species are expressed via precocial male maturation, a rare mode of strategy expression in insects. Additionally, adult lifespans differed significantly among morphs with 8th instar males having the shortest, and 9th instar males having the longest lifespans. I discuss how these differences in lifespan align with morph-specific investment in pre- and post-copulatory processes to equalize fitnesses among morphs.

Behavioural differences in predator aware and predator naïve Wellington tree wētā, Hemideina crassidens.

Insects have evolved a wide range of behavioural traits to avoid predation, with anti-predator behaviours emerging as important adaptive responses to the specific strategies employed by predators. These responses may become ineffective, however, when a species is introduced to a novel predator type. When individuals cannot recognise an introduced predator for instance, they may respond in ways that mean they fail to avoid, escape, or neutralize a predator encounter. New Zealand's endemic insect fauna evolved in the absence of terrestrial mammalian predators for millions of years, resulting in the evolution of unique fauna like the large, flightless Orthopteran, the wētā. Here we investigate how experience with introduced mammalian predators might influence anti-predator behaviours by comparing behaviours in a group of Wellington tree wētā (Hemideina crassidens) living in an ecosanctuary, Zealandia, protected from non-native mammalian predators, and a group living in adjacent sites without mammalian predator control. We used behavioural phenotyping assays with both groups to examine rates of activity and defensive aggression shortly after capture, and again after a period of acclimation. We found that wētā living in protected areas were more active shortly after capture than wētā in non-protected habitats where mammalian predators were present. Male wētā living in non-protected areas tended to be less aggressive than any other group. These results suggest that lifetime experience with differing predator arrays may influence the expression of antipredator behaviour in tree wētā. Disentangling innate and experiential drivers of these behavioural responses further will have important implications for insect populations in rapidly changing environments.

Equal fitness among alternative mating strategies in a harem polygynous insect.

Alternative mating strategies are widespread among animal taxa, with strategies controlled by a genetic polymorphism (Mendelian strategy) being rarer in nature than condition-dependent developmental strategies. Mendelian strategies are predicted to have equal average fitnesses and the proportion of offspring produced by a strategy should equal the equilibrium proportion of individuals representing the strategy in a population. Developmental strategies are not expected to produce offspring in equilibrium proportions; however, whether the alternative phenotypes should have equal average fitness is debated. The Wellington tree wētā (Hemideina crassidens) (Orthoptera: Anostostomatidae) is a harem polygynous insect in which intense sexual competition has favoured the evolution of three alternative mating strategies that differ in weapon size and the ability to fight for control of harems. Here, we use molecular genotyping to test the hypothesis that the alternative strategies in this species are maintained by having equal relative fitness and that morphs produce offspring in equilibrium proportions. As expected, the average relative fitness of the three strategies did not significantly differ and the proportion of offspring produced by each morph is equal to the frequency of that morph in the population. Our results support the hypothesis that the alternative male morphs in H. crassidens represent Mendelian strategies.

Benefits of multiple mating in a sexually dimorphic polygynandrous insect

Mating with multiple partners is common across animal taxa. Males mate multiply because reproductive success positively correlates with mating success. In contrast, multiple mating is expected to increase the direct (material) or indirect (genetic) benefits accrued by females but not necessarily increase their reproductive success. Cases in which female reproductive success increases with mating success could be due to females acquiring material resources that directly increase reproductive output. Because multiple mating likely increases reproductive success more in males than in females, males typically experience greater sexual selection. Consequently, males in harem polygynous species, where a few males can monopolize access to several females in a population, are expected to be under stronger sexual selection than females. We field-test these predictions by using the harem polygynous Wellington tree wētā, Hemideina crassidens. Here, we develop microsatellite markers for H. crassidens and use them to genotype females, their offspring and putative sires to estimate the opportunity for selection as well as quantify natural rates of multiple mating and its effect on male and female reproductive success (number of hatchlings). We found that both sexes mate multiply and that reproductive success increases with mating success in both sexes. Males and females have similar total opportunities for selection, and sexual selection comprises approximately 50% of the total selection operating in males. We found that female oviposition rate increases with mating success, but we found no evidence to support the hypothesis that females derive indirect benefits from polyandry. Our study provides strong evidence that male and female H. crassidens derive significant direct fitness benefits from multiple mating under natural conditions.

Sub-lethal exposure to a mammalian pesticide bait alters behaviour in an orthopteran

Pesticides are a crucial tool to control introduced pest species, facilitating restoration of native ecosystems and reducing mortality risk in endemic species. However, non-target species, including many invertebrates, consume pesticides. Although lethal effects on these non-target species are often documented, sub-lethal effects are poorly understood. New Zealand presents a unique case study in this field, with a range of introduced mammalian pest species that threaten a large proportion of endemic fauna. Current research suggests that vertebrate pesticide baits do not cause mortality in invertebrate consumers, but few studies investigate sub-lethal behavioural effects. In this study, we tested whether consumption of a widely dispersed anticoagulant rodenticide, brodifacoum, influenced the expression and repeatability of behaviour in a known consumer of the bait, Wellington tree weta (Hemideina crassidens) over a 40-day treatment period. We compared refuge emergence, activity, refuge-seeking tendencies and defensive responses of brodifacoum-exposed and untreated control weta. Bait-exposed individuals showed increased emergence but decreased activity, boldness and aggression compared to untreated controls. These results show that brodifacoum, although not directly causing mortality, may alter behaviours directly related to foraging, mating, competitive interactions and anti-predator responses, which could be detrimental to fitness and survival. More research should be undertaken to investigate the capacity for H. crassidens to tolerate exposure, and to determine any age- or duration-related responses. These results should also be a catalyst for further research on non-target behavioural effects in other pesticide-exposed insect species.

Do alternative reproductive strategies in the Wellington tree weta represent different behavioural types?

AbstractIn many animal species, variation in reproductive success among individuals has led to the evolution of alternative mating strategies, which in the case of insects can often be correlated with developmental trajectories. In the Wellington tree weta, Hemideina crassidens, males can mature at the 8th, 9th or 10th instar, while females mature at the 10th instar only. A number of morphological attributes including male head and mandible size correlate with final instar number, and as these attributes represent a form of weaponry, they are often used in mate/site guarding and male–male competition. Tenth instar males have larger head/mandible/body sizes and show a conventional (guarder) reproductive strategy, whereas smaller 8th instar males typically show an unconventional (sneaker) strategy. In contrast, 9th instar males are predicted to adopt a “jack‐of‐all‐trades” strategy whereby they can fight or sneak depending context. Here, we tested whether alternative reproductive morphs exhibit strategy‐specific differences in risk‐taking associated with refuge emergence, activity and antipredator behaviour and further, whether these traits correlate to form a behavioural syndrome. We found that tree weta show consistent and repeatable differences in activity and refuge use at the individual level; however, behavioural covariances suggest that only 8th instar males exhibit a behavioural syndrome. That 9th instar males show high plasticity and variance in their gallery‐related behaviours supports the hypothesis that these males are a “jack‐of‐all‐trades.” Contrary to our predictions, antipredator behaviour was not correlated with other traits, and differences in behaviour overall were consistently more pronounced between individuals rather than between male morphs or sexes.

Refuge size variation and potential for sperm competition in Wellington tree weta.

Ecological variation in resources can influence the distribution and encounter rates of potential mates and competitors and, consequently, the opportunity for sexual selection. Factors that influence the likelihood that females mate multiply could also affect the potential for sperm competition. In Wellington tree weta (Hemideina crassidens, plural “weta”), the size of tree cavities (called galleries) used as refuges affects weta distribution and thus the opportunity for sexual selection and selection on male weaponry size. We examined the predicted effects of gallery size and male weaponry size on the potential for sperm competition. We asked if gallery size influenced the potential for multiple mating by females and potential for sperm competition, if male weaponry size was associated with relative expected sperm competition intensity (SCI), and if estimated male mating success was correlated with potential SCI. To quantify relative competitive environments of males, we created and analyzed networks of potential competitors based on which males could have mated with the same females. We found that small galleries had higher potential for female multiple mating and higher potential for sperm competition. Size of male weaponry was not associated with expected relative SCI. Regardless of gallery size, males with more potential mates were expected to face lower expected relative sperm competition. Thus, in this system, variation in the size of available refuges is likely to influence the potential for sperm competition, in a way that we might expect to increase variation in overall reproductive success.

Successful use of radiotransmitters in tracking male tree wētā Hemideina crassidens (Orthoptera: Tettigonioidea: Anostostomatidae)

ABSTRACTRadiotransmitters have been used successfully to track and recapture giant wētā (Deinacrida species) in part to assess mating success. We report the successful use of very light transmitters (0.2 g) to track male Wellington tree wētā, Hemideina crassidens, over several nights to daytime refuges in burrows and tree galleries. Male Hemideina species sport lengthy mandibles used as weapons in fights with rivals over groups of females living in gallery refuges. Consistent with previous studies showing that males with the longest mandibles cohabit with the largest groups of females, our two largest radio-tagged males were the only ones relocated with adult females.

Explaining large mitochondrial sequence differences within a population sample.

Mitochondrial DNA sequence is frequently used to infer species' boundaries, as divergence is relatively rapid when populations are reproductively isolated. However, the shared history of a non-recombining gene naturally leads to correlation of pairwise differences, resulting in mtDNA clusters that might be mistaken for evidence of multiple species. There are four distinct processes that can explain high levels of mtDNA sequence difference within a single sample. Here, we examine one case in detail as an exemplar to distinguish among competing hypotheses. Within our sample of tree wētā (Hemideina crassidens; Orthoptera), we found multiple mtDNA haplotypes for a protein-coding region (cytb/ND1) that differed by a maximum of 7.9%. From sequencing the whole mitochondrial genome of two representative individuals, we found evidence of constraining selection. Heterozygotes were as common as expected under random mating at five nuclear loci. Morphological traits and nuclear markers did not resolve the mtDNA groupings of individuals. We concluded that the large differences found among our sample of mtDNA sequences were simply owing to a large population size over an extended period of time allowing an equilibrium between mutation and drift to retain a great deal of genetic diversity within a single species.

Sexually dimorphic effect of mating on the melanotic encapsulation response in the harem‐defending Wellington tree weta, Hemideina crassidens (Orthoptera: Tettigonioidea: Anostostomatidae)

AbstractReproductive activities are generally costly to immune responsiveness because limited resources required by reproduction are diverted away from immunity (and vice versa). Reproduction, however, is not expected to affect the immune response in males and females similarly as mating is expected to negatively affect male immunity more so than female immunity. Here, I test the phenotypic plasticity hypothesis in the Wellington tree weta (Hemideina crassidens), a sexually dimorphic orthopteran insect that is endemic to New Zealand. My laboratory experiment showed that although males had higher rates of melanotic encapsulation than females, contrary to prediction, females were the only sex significantly affected by mating and the effect was positive. In addition to immunity differing between the sexes, immune function can differ intrasexually, particularly when males are polymorphic and different investment strategies are used to maximize fitness. Male H. crassidens exhibit alternative mating strategies that are represented by three different morphotypes. I therefore explored whether the morphs differed in their melanotic encapsulation response and whether mating affected the morphs differently. I found no difference among morphs or an effect of mating on male immune response.

Water loss in tree weta (Hemideina): adaptation to the montane environment and a test of the melanisation-desiccation resistance hypothesis.

Montane insects are at a higher risk of desiccation than their lowland counterparts and are expected to have evolved reduced water loss. Hemideina spp. (tree weta; Orthoptera: Anostostomatidae) have both lowland (Hemideina femorata, Hemideina crassidens and Hemideina thoracica) and montane (Hemideina maori and Hemideina ricta) species. H. maori has both melanic and yellow morphs. We use these weta to test two hypotheses: that montane insects lose water more slowly than lowland species, and that cuticular water loss rates are lower in darker insects than lighter morphs, because of incorporation of melanin in the cuticle. We used flow-through respirometry to compare water loss rates among Hemideina species and found that montane weta have reduced cuticular water loss by 45%, reduced respiratory water loss by 55% and reduced the molar ratio of V̇H2 O:V̇CO2 by 64% compared with lowland species. Within H. maori, cuticular water loss was reduced by 46% when compared with yellow morphs. Removal of cuticular hydrocarbons significantly increased total water loss in both melanic and yellow morphs, highlighting the role that cuticular hydrocarbons play in limiting water loss; however, the dark morph still lost water more slowly after removal of cuticular hydrocarbons (57% less), supporting the melanisation-desiccation resistance hypothesis.

Comparative cytogenetics of North Island tree wētā in sympatry

In North Island New Zealand three species of tree wētā (Hemideina) have narrow regions of overlap. Using detailed measurements of chromosomes we compared the karyotypes of Hemideina thoracica with those of Hemideina crassidens and Hemideina trewicki. Although H. thoracica and H. trewicki have the same diploid number (2n = 17 [XO], 18 [XX]), distinct from H. crassidens (2n = 15 [XO] 16 [XX]); the karyotypes of H. trewicki and H. crassidens are more similar to each other than either is to H. thoracica. Elements within each karyotype were identified that are species specific and will aid identification of putative hybrids. Quantitative cytogenetics was used to identify the sex chromosome for H. crassidens and H. trewicki, which in contrast to previous inferences, is most likely the fifth-longest metacentric chromosome in H. crassidens, and the third-longest metacentric chromosome in H. trewicki.

Elevational variation in adult body size and growth rate but not in metabolic rate in the tree weta Hemideina crassidens

Populations of the same species inhabiting distinct localities experience different ecological and climatic pressures that might result in differentiation in traits, particularly those related to temperature. We compared metabolic rate (and its thermal sensitivity), growth rate, and body size among nine high- and low-elevation populations of the Wellington tree weta, Hemideina crassidens, distributed from 9 to 1171ma.s.l across New Zealand. Our results did not indicate elevational compensation in metabolic rates (metabolic cold adaptation). Cold acclimation decreased metabolic rate compared to warm-acclimated individuals from both high- and low-elevation populations. However, we did find countergradient variation in growth rates, with individuals from high-elevation populations growing faster and to a larger final size than individuals from low-elevation populations. Females grew faster to a larger size than males, although as adults their metabolic rates did not differ significantly. The combined physiological and morphological data suggest that high-elevation individuals grow quickly and achieve larger size while maintaining metabolic rates at levels not significantly different from low-elevation individuals. Thus, morphological differentiation among tree weta populations, in concert with genetic variation, might provide the material required for adaptation to changing conditions.

Effect of an immune challenge on the functional performance of male weaponry

Theories of parasite-mediated sexual selection predict a positive association between immune function and the expression of sexually selected ornaments. Few studies, however, have investigated how an immune challenge affects the performance of sexually selected weaponry. Male Wellington tree weta (Hemideina crassidens) (Orthoptera: Anostostomatidae) possess enlarged mandibles that are used as weapons in fights for access to females residing in tree galleries. Intense sexual competition appears to have favoured the evolution of alternative male mating strategies in this species as males have a trimorphic phenotype in which weapon size varies across morphotype: 8th instar males have the smallest jaws, 10th instar males have the largest and 9th instar males being intermediate to the other two. After injecting males and females with either lipopolysaccharide (LPS; immune challenge) or saline (control) I measured over a 24h period each weta's body mass to assess whether they responded immunologically to the LPS and their bite force to assess the functional performance of their jaws. Both sexes responded immunologically to the immune-challenge as LPS-injected individuals lost significantly more body mass than saline-injected controls with females losing more mass than males. Female bite force was significantly reduced 8h after LPS-injection whereas male bite force did not significantly decline. Both sexes regained pre-injection functional performance of their jaws 24h after the immune challenge. My results suggest that females trade-off bite force for immune function whereas males do not.This article is part of a Special Issue entitled: insert SI title.

Convergent local adaptation in size and growth rate but not metabolic rate in a pair of parapatric Orthoptera species

Local adaptation is inferred for many morphological and physiological traits but determining the role of natural selection in shaping geographical variation relies on evidence such as provided by fitness estimates or transplantation experiments. In addition, habitat-specific convergent (or parallel) evolution provides a powerful means of testing adaptive hypotheses. In the present study, we contrast size, growth rate, and metabolic rate (as inferred by oxygen consumption) in a pair of Orthopteran species collected from high and low altitude locations and raised in identical environments. We find that two related insects (tree wētā: Hemideina crassidens and Hemideina thoracica) have the same (convergent) pattern of larger adults and faster growth rates in populations from a high altitude location compared to conspecifics from low altitude. However, variation in metabolic rate was detected only between species and not among altitudes. The high and low altitude populations of each species were collected from the same location; therefore, selection pressures on the two species are likely to be similar. Thus, the independent detection of larger adults and faster growth rate of wētā derived from high altitude suggests an adaptive role for both these traits in tree wētā. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 123–135.

Tolerance for nutrient imbalance in an intermittently feeding herbivorous cricket, the Wellington tree weta.

Organisms that regulate nutrient intake have an advantage over those that do not, given that the nutrient composition of any one resource rarely matches optimal nutrient requirements. We used nutritional geometry to model protein and carbohydrate intake and identify an intake target for a sexually dimorphic species, the Wellington tree weta (Hemideina crassidens). Despite pronounced sexual dimorphism in this large generalist herbivorous insect, intake targets did not differ by sex. In a series of laboratory experiments, we then investigated whether tree weta demonstrate compensatory responses for enforced periods of imbalanced nutrient intake. Weta pre-fed high or low carbohydrate: protein diets showed large variation in compensatory nutrient intake over short (<48 h) time periods when provided with a choice. Individuals did not strongly defend nutrient targets, although there was some evidence for weak regulation. Many weta tended to select high and low protein foods in a ratio similar to their previously identified nutrient optimum. These results suggest that weta have a wide tolerance to nutritional imbalance, and that the time scale of weta nutrient balancing could lie outside of the short time span tested here. A wide tolerance to imbalance is consistent with the intermittent feeding displayed in the wild by weta and may be important in understanding weta foraging patterns in New Zealand forests.

Reproductive and physiological costs of repeated immune challenges in female Wellington tree weta (Orthoptera: Anostostomatidae)

Fitness-related traits, such as immunity and reproduction, are typically condition dependent, and are predicted to trade off against each other because they share a pool of energy and resources. It is generally assumed that the resources and energy required for immune processes and reproduction is contained in the body fat; however, few studies quantify the effect of an immune insult on fat load. I tested the hypothesis that if mounting an immune response is physiologically costly in terms of consuming limited resources from body fat, and reproduction also relies on these resources, then an immune challenge should cause a reduction in fat load and an associated decline in reproduction. I tested this hypothesis by assaying the fat content of female Wellington tree weta (Hemideina crassidens) after repeated challenges with lipopolysaccharide (LPS), and counting the number of oviposited eggs in addition to assaying the egg protein content, a possible measure of egg quality. In line with my prediction, immune-challenged females had significantly smaller fat loads and laid significantly fewer eggs than saline-injected controls. Moreover, the protein content of the eggs laid by immune-challenged females was significantly lower than that of controls. My experimental results show that an immune challenge with a non-pathogenic stimulant increases fat consumption, which in turn limits the resources available for reproduction. These findings support the hypothesis that reproduction and immunity are condition dependent, and are traded off against each other. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104, 38–46.

What weta want: colour preferences of a frugivorous insect

Plants use colours as signals to attract mutualists and repel antagonists. Fleshy-fruits are often conspicuously coloured to signal different types of information including fruit maturity and spatial location. Previous work on fruit colour selection focus on large diurnal vertebrates, yet fruit colours are perceived differently by frugivores with different types of visual systems. Here, we tested whether a nocturnal, frugivorous, seed-dispersing insect selects fruits based on their pigmentation and whether different lighting conditions affect fruit colour selection. We captured 20 Wellington tree weta (Hemideina crassidens) from a forest reserve on the North Island of New Zealand and brought them into laboratory conditions to test their fruit colour preferences. The fruits of Coprosma acerosa, a native shrub species that naturally produces translucent, blue-streaked fruits, were dyed either red or blue. Fruits were then offered to weta in a binary (y-maze) choice test in two light conditions, either at night during a full moon or under artificial light conditions in the lab. Weta preferred unmanipulated, naturally blue-streaked fruits and artificially-blue coloured fruits over those dyed red. Furthermore, their colour preferences were unaffected by light environment. Our results therefore suggest that weta can discriminate between colours (using colour vision) in both light and dark light environments. Their consistent preferences for colours other than red indicate that weta might be responsible for the unusual colours of fleshy-fruits in New Zealand.

Sexual Selection, Ontogenetic Acceleration, and Hypermorphosis Generates Male Trimorphism in Wellington Tree Weta

Strong sex-specific selection on traits common to both sexes typically results in sexual dimorphism. Here we find that Wellington tree weta (Hemideina crassidens) are sexually dimorphic in both head shape and size due to differential selection pressures on the sexes: males use their heads in male-male combat and feeding whereas females use theirs for feeding only. Remarkably, the sexes share a common ontogenetic trajectory with respect to head growth. Male head shape allometry is an extension of the female’s trajectory despite maturing two instars earlier, a feat achieved through ontogenetic acceleration and hypermorphosis. Strong sexual selection also favours the evolution of alternative reproductive strategies in which some males produce morphologically different weapons. Wild-caught male H. crassidens are trimorphic with regard to weapon size, a rare phenomenon in nature, and weapon shape is related to each morph’s putative mating strategy.

Sexually dimorphic immune response in the harem polygynous Wellington tree weta Hemideina crassidens

Abstract Adult males are often less immunocompetent than females. One explanation for this is that intense sexual selection causes males to trade‐off investment in immunity with traits that increase mating success. This hypothesis is tested in the Wellington tree weta (Hemideina crassidens), a large, sexually dimorphic orthopteran insect in which males possess enormous mandibular weaponry used during fights for access to female mates. Field‐collected males have a significantly greater immune response (greater melanotic encapsulation) than females, suggesting that body condition, longevity or an allied trait is important to male fitness, or that females require materials for egg production that would otherwise be used to boost immunity. Although immunity is expected to trade‐off against reproductive traits in both sexes, there is no significant relationship between immune response and weapon or testes size in males, nor fecundity in females.