Susceptibility and behavioral responses of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae

Termites exploit microbially rich resources such as decayed wood and soil that are colonized by potentially pathogenic and parasitic fungi, bacteria, viruses, and nematodes. In colonies composed of thousands of individuals, the risk of infection among nestmates is significant, and individual and social behavior could involve various adaptations to resist disease and parasitism. Here we show that the dampwood termite Zootermopsis angusticollis (Hagen) exhibits a dosage dependent susceptibility to the soil nematode Steinernema carpocapsae (Weiser) (Mexican strain) and that this social insect significantly alters its behavior in response to this entomopathogenic roundworm. Relative to their baseline behavior, termites exposed to infective juveniles increased the frequency and duration of allogrooming and vibratory displays as well as two other novel behaviors, abdominal tip-raising and self-scratching. Whereas the first two behaviors likely reflect general adaptations to reduce susceptibility to a variety of pathogens and parasites, the latter behaviors might be specific to nematodes because they have never been observed in Z. angusticollis in any other pathogenic context. Our results support the hypotheses that behavioral responses in termites are important in the control of pathogenic and parasitic microorganisms and that termite susceptibility is socially mediated.     

Phenotypes optimized for early‐life reproduction exhibit faster somatic deterioration with age,revealing a latent cost of high condition

High condition enables individuals to express a phenotype with greater reproductive potential. However, life‐history theory predicts that reproduction will trade off with somatic maintenance and viability, and several studies have reported faster age‐related decline in performance in high‐condition individuals, suggesting that high condition in early life is associated with accelerated somatic deterioration. This trade‐off may be especially pronounced in males, which often express condition‐dependent secondary sexual traits that can impose viability costs during development and through damage‐inflicting adult sexual behaviours. To test this prediction, we reared larvae of the neriid fly Telostylinus angusticollis on diets of varying nutrient content and quantified somatic deterioration in solitary males, males housed in all‐male or mixed‐sex groups and immobilized males subjected to mechanical stress. We found that males reared on a nutrient‐rich larval diet (high‐condition males) suffered a higher rate of somatic deterioration with age, particularly when housed in groups. Perhaps as a result of accelerated somatic deterioration, high‐condition males did not outlive low‐condition males. In addition, high‐condition males housed in all‐male groups experienced a greater reduction in escape response with age than males housed in mixed‐sex groups, suggesting that male–male combat promotes somatic deterioration. However, even when immobilized, high‐condition males were still found to be more susceptible to somatic damage than low‐condition males. Our findings suggest that a high‐condition male phenotype is more prone to somatic damage, both as a result of associated behaviours such as combat, and because of the inherent fragility of the high‐condition body.     

Convergent evolution of sexual shape dimorphism in Diptera

Several patterns of sexual shape dimorphism, such as male body elongation, eye stalks, or extensions of the exoskeleton, have evolved repeatedly in the true flies (Diptera). Although these dimorphisms may have evolved in response to sexual selection on male body shape, conserved genetic factors may have contributed to this convergent evolution, resulting in stronger phenotypic convergence than might be expected from functional requirements alone. I compared phenotypic variation in body shape in two distantly related species exhibiting sexually dimorphic body elongation: Prochyliza xanthostoma (Piophilidae) and Telostylinus angusticollis (Neriidae). Although sexual selection appears to act differently on male body shape in these species, they exhibited strikingly similar patterns of sexual dimorphism. Likewise, patterns of within-sex shape variation were similar in the two species, particularly in males: relative elongation of the male head capsule, antenna, and legs was associated with reduced head capsule width and wing length, but was nearly independent of variation in thorax length. However, the two species presented contrasting patterns of static allometry: male sexual traits exhibited elevated allometric slopes in T. angusticollis, but not in P. xanthostoma. These results suggest that a shared pattern of covariation among traits may have channeled the evolution of sexually dimorphic body elongation in these species. Nonetheless, static allometries may have been shaped by species-specific selection pressures or genetic architectures.     

Social influence of larvae on ovarian maturation in primary and secondary reproductives of the dampwood termite Zootermopsis angusticollis

We tested the effect of larvae on the reproductive maturation and fecundity of female primary and secondary reproductives of the termite Zootermopsis angusticollis Hagen (Isoptera; Termopsidae) by varying the number of third‐ to fourth‐instar larvae nesting with heterosexually paired reproductives. Primary females had higher fecundities and oviposited sooner when nesting with larvae than females lacking larvae, but gained less body mass and had fewer functional ovarioles per ovary. Secondary reproductives nesting with larvae also had higher fecundities and oviposited sooner, but unlike primaries, they gained more body mass and had more functional ovarioles when larvae were present. The specific response of both primary and secondary females varied according to the number of larvae present. These results suggest that larvae can enhance the fecundity of primary and secondary females. Larvae may increase the energetic reserves of reproductives by performing colony labour, reducing pathogen load and providing trophallactic secretions. Trophallaxis with larvae may significantly enhance endogenous nitrogen, which is a limiting nutrient for termites. Primary females, which normally need to produce a first brood quickly to initiate a new colony, may expend limited nutritional resources on oogenesis rather than producing additional ovarioles. Primaries may also store fewer energetic reserves for long‐term brood care, and therefore gained less mass when larvae were present to attend to non‐reproductive tasks. Secondary females may exhibit a greater positive response to larvae than primaries because they begin reproductive life with fewer stored resources and thus their development and fecundity are more dependent on assistance from larvae. Both primary and secondary reproductives may become more dependent on the contributions of larvae as their rate of egg production increases with subsequent bouts of oviposition.     

The dissimilar costs of love and war: age-specific mortality as a function of the operational sex ratio

Lifespan and ageing are strongly affected by many environmental factors, but the effects of social environment on these life-history traits are not well understood. We examined effects of social interaction on age-specific mortality rate in the sexually dimorphic neriid fly Telostylinus angusticollis. We found that although interaction with other individuals reduced longevity of both sexes, the costs associated with variation in operational sex ratio were sex specific: males' early-life mortality rate increased, and lifespan decreased, with increasing male bias in the sex ratio, whereas surprisingly, the presence of males had no effect on early-life mortality or lifespan of females. Intriguingly, early-life (immediate) mortality costs did not covary with late-life (latent) costs. Rather, both sexes aged most rapidly in a social environment dominated by the opposite sex. Our findings suggest that distinct reproductive activities, such as mating and fighting, impose different age-specific patterns of mortality, and that such costs are strongly sex specific.     

Maternal and paternal condition effects on offspring phenotype in Telostylinus angusticollis (Diptera: Neriidae)

It is widely recognized that maternal phenotype can have important effects on offspring, but paternal phenotype is generally assumed to have no influence in animals lacking paternal care. Nonetheless, selection may favour the transfer of environmentally acquired condition to offspring from both parents. Using a split-brood, cross-generational laboratory design, we manipulated a key environmental determinant of condition - larval diet quality - of parents and their offspring in the fly Telostylinus angusticollis, in which there is no evidence of paternal provisioning. Parental diet did not affect offspring survival, but high-condition mothers produced larger eggs, and their offspring developed more rapidly when on a poor larval diet. Maternal condition had no effect on adult body size of offspring. By contrast, large, high-condition fathers produced larger offspring, and follow-up assays showed that this paternal effect can be sufficient to increase mating success of male offspring and fecundity of female offspring. Our findings suggest that both mothers and fathers transfer their condition to offspring, but with effects on different offspring traits. Moreover, our results suggest that paternal effects can be important even in species lacking conventional forms of paternal care. In such species, the transfer of paternal condition to offspring could contribute to indirect selection on female mate preferences.     

Microsatellite markers for two species of dampwood termites in the genus Zootermopsis (Isoptera: Termopsidae)

Dampwood termites in the genus Zootermopsis inhabit forested areas in western North America. To better understand the colony composition and breeding structure of Zootermopsis, we identified polymorphic microsatellite loci to use in population analysis. Microsatellite loci were isolated from Zootermopsis nevadensis nevadensis (Hagen); however, all primers amplified homologous loci in Zootermopsis angusticollis (Hagen) and Zootermopsis nevadensis nuttingi (Hagen). Twelve loci were polymorphic in one or more of the above subspecies and species. The number of alleles per locus ranged from one to six, with some allelic differences among subspecies and species. We are currently utilizing the microsatellite markers to investigate the population genetics of Zootermopsis.     

THE SPERMATOZOON OF ARTHROPODA: ZOOTERMOPSIS NEVADENSIS AND ISOPTERAN SPERM PHYLOGENY

In this paper, the ultrastructure of the spermatozoon of Zootermopsis nevadensis (Isoptera, Hodotermitidae) and of some Rhinotermitidae and Termitidae is described. Zootermopsis sperm is rod like, aflagellate, immotile, and without an acrosome; it is composed of a filiform nucleus encircled by a monolayered microtubular manchette, and a few mitochondria. This spermatozoon was previously thought to be flagellate, and therefore the most primitive in Isoptera: our present study suggests a new phylogenetical position for Hodotermitidae. All the species of Rhinotermitidae and Termitidae studied by us show a similar spheroidal sperm model, devoid of acrosome, flagellum and manchette at spermatid stage, and are made up of only a round nucleus, two mitochondria and a centriole. This widely distributed model seems to be the more evolved in the order. The nature of sperm evolution in the Isoptera is considered.     

Condition dependence of developmental stability in the sexually dimorphic fly Telostylinus angusticollis (Diptera: Neriidae)

Developmental stability is widely regarded as a condition‐dependent trait, but its relation to genotype and environment, and extent of developmental integration, remain contentious. In Telostylinus angusticollis, the dorsocentral bristles exhibit striking variation in developmental stability, manifested as fluctuating asymmetry (FA) in bristle position (‘positional FA’) and failure to develop some bristles (‘bristle loss’), in natural and laboratory populations. To determine whether this variation reflects condition, I tested for effects of genotype and environment (larval diet quality), and examined covariation with condition‐dependent traits. Positional FA was not affected by genotype or environment. However, positional FA covaried negatively with secondary sexual trait expression in males, and with sexual dimorphism in body shape, but covaried positively with body size in females. Bristle loss reflected both genotype and larval diet. Flies reared on poor‐quality diet exhibited a similar rate of bristle loss as wild flies. Both positional FA and bristle loss were greater in males. These results suggest that the relation between developmental stability and condition is complex and sex dependent.     

Cyclic carbon dioxide release in the dampwood termite, Zootermopsis nevadensis (Hagen)

Real-time traces of CO₂ release of pseudergates of the dampwood termite, Zootermopsis nevadensis (Hagen) were obtained using flow-through respirometry. Traces were made at each of six temperatures, between 10 and 35°C. Termites released CO₂ in a cyclic pattern at each of the six temperatures. CO₂ release rate (as in ml h⁻¹) increased significantly with temperature and body mass. Rate of change in with temperature (or Q₁₀) was 2.11. Degree of cycling in CO₂ traces was estimable using the coefficient of variability. Coefficient of variability for both acyclic and cyclic traces declined exponentially with increasing temperature.