Host–enemy interactions provide limited biotic resistance for a range-expanding species via reduced apparent competition

Aim

As species' ranges shift poleward in response to anthropogenic change, they may lose antagonistic interactions if they move into less diverse communities, fail to interact with novel populations or species effectively, or if ancestral interacting populations or species fail to shift synchronously. We leveraged a poleward range expansion in a tractable insect host–enemy community to uncover mechanisms by which altered antagonistic interactions between native and recipient communities contributed to ‘high niche opportunities’ (limited biotic resistance) for a range-expanding insect.

Location

North America, Pacific Northwest.

Methods

We created quantitative insect host–enemy interaction networks by sampling oak gall wasps on 400 trees of a dominant oak species in the native and expanded range of a range-expanding gall wasp species. We compared host–enemy network structure between regions. We measured traits (phenology, morphology) of galls and interacting parasitoids, predicting greater trait divergence in the expanded range. We measured function relating to host control and explored if altered interactions and traits contributed to reduced function, or biotic resistance.

Results

Interaction networks had fewer species in the expanded range and lower complementarity of parasitoid assemblages among host species. While networks were more generalized, interactions with the range-expanding species were more specialized in the expanded range. Specialist enemies effectively tracked the range-expanding host, and there was reduced apparent competition with co-occurring hosts by shared generalist enemies. Phenological divergence of enemy assemblages interacting with the range-expanding and co-occurring hosts was greater in the expanded range, potentially contributing to weak apparent competition. Biotic resistance was lower in the expanded range, where fewer parasitoids emerged from galls of the range-expanding host.

Main Conclusions

Changes in interactions with generalist enemies created high niche opportunities, and limited biotic resistance, suggesting weak apparent competition may be a mechanism of enemy release for range-expanding insects embedded within generalist enemy networks.     

Weak interactions between avian and insect frugivores: the case of Pistacia terebinthus L. (Anacardiaceae)

Vertebrate frugivores often feed on fruits upon or within which insects also feed, yet little information exists on the potential magnitude of interactions between these consumers. The Mediterranean shrub Pistacia terebinthus, the birds that consume its fruits, and the wasps that feed upon its seeds are examined in this study. P. terebinthus produces a highly variable fraction of final-sized red fruits that never become mature (green-colored). Red fruits can be immature, parthenocarpic, aborted, or attacked by wasps, and their pulp is much less nutritious than that of mature fruits. A total of 20 bird species consumed the fruits in the study area. Legitimate dispersers accounted for 39% of the total fruit removal, while pulp eaters and seed predators accounted for the remainder. Birds strongly preferred the mature fruits (only 4% of the fruits consumed were red). The incidence of wasps in the seeds ranged from 0 to 42% of the crop in 1989 and from 0 to 24% in 1990. The influence of avian and insect frugivore guilds on each other appears to be quite low because of the narrow overlap in resource utilization by birds and wasps, and an overall low intensity of wasp seed predation. From an evolutionary perspective, the possible ability of wasps to preclude fruit maturation appears not to be attributable to the present interaction with avian frugivores.     

Species and Colony Components in the Recognition Odor of Young Social Wasps: Their Expression and Learning (Polistes biglumis and P. atrimandibularis; Hymenoptera: Vespidae)

In Polistes, nestmate recognition relies on the learning of recognition cues from the nest. When wasps recognize nestmates, they match the template learned with the odor of the encountered wasp. The social wasp Polistes biglumis use the homogeneous odor of their colony to recognize nestmates. When these colonies become host colonies of the social parasite P. atrimandibularis, colony odor is no longer homogeneous, as the parasite offspring have an odor that differs from that of their hosts. In trying to understand how the mechanism of nestmate recognition works in parasitized colonies and why parasite offspring are accepted by hosts, we tested the responses of resident Polistes biglumis wasps from parasitized and unparasitized colonies to newly emerged parasites and to nestmate and non-nestmate conspecifics. The experiments indicate that immediately upon eclosion both young parasites and young hosts lack a colony odor and that colony odor can be soon acquired from the accepting colony. In addition, while residents of nonparasitized colonies recognize only the odor of their species, resident hosts of parasitized colonies have learned a template that fits the odors of two species.     

Ultrastructural features of the hypopharyngeal glands in the social wasp Polistes versicolor (Hymenoptera: Vespidae)

The wasps of the genus Polistes have been considered the key to understanding the evolution of social behavior in Hymenoptera. Several studies have shown that the development of organized insect societies was accompanied by the evolution of structures like exocrine glands, which became specialized to perform specific functions. This article investigates the ultrastructural and cytochemical features of the hypopharyngeal glands of Polistes versicolor. These glands have been studied in depth in social bees, where they occur only in nurses and produce the royal jelly. Our results revealed that these glands basically did not vary among individuals or between sexes. They are constituted by spherical cells, each with a large nucleus and well‐developed rough endoplasmic reticulum. Secretion vesicles are abundant, but lipid droplets were not observed, indicating that these glands may not have a role in pheromone synthesis. Acid phosphatase was detected in lysosomes, and also free in the cytosol, but did not seem to be related with cell death. Thus, our results suggest that the hypopharyngeal glands of P. versicolor may not have a specialized social role, but could produce digestive enzymes.     

Mating system and population structure of the primitively eusocial wasp Ropalidia revolutionalis: a model system for the evolution of complex societies

Mating systems are important determinants of genetic structure in cooperative groups, and their effects can influence profoundly the interactions of group members. The primitively eusocial wasp, Ropalidia revolutionalis, has an interesting genetic and social structure that makes it an excellent model system for examining the evolution of more complex societies. In particular, its colonies sometimes have multiple queens, a key characteristic of more advanced wasp societies. In this study, we have characterized the mating system of the social wasp Ropalidia revolutionalis to understand better its colony genetic structure. R. revolutionalis females nearly always mate singly and they are unrelated to their mates. However, different females in the same colony do mate with males, on average, who are related as cousins. Single mating will help to maintain high relatedness, which should be important for continued cooperation in multiple queen societies, but it creates potential conflicts in single queen colonies over the production of males as well as over the timing of male production. We have also characterized the population structure of R. revolutionalis from Townsville, in tropical north Queensland, to Brisbane in the subtropics. Even at such a large scale, the population is remarkably unstructured with an average F(ST) of 0.0546. There is weak isolation by distance, and evidence for subtle differentiation between a southern region with no dry season, which extends as far north as Rockhampton, and a northern region with a severe to moderate dry season. This may reflect historical effects of extreme aridity on the population structure.     

Cuticular hydrocarbon dynamics in young adult Polistes dominulus (Hymenoptera: Vespidae) and the role of linear hydrocarbons in nestmate recognition systems

In social insects, cuticular hydrocarbons (CHCs) play an important role in nestmate discrimination processes, but young individuals are usually not discriminated. We studied CHC changes in young workers of the social wasp Polistes dominulus. A quantitative estimation demonstrated that total quantities of CHCs increased after emergence, with branched alkanes increasing drastically when compared with other classes of hydrocarbons. The relative quantity of longer-chain compounds increased with respect to shorter ones; unsaturated compounds decreased. These changes might reduce the capacity of the cuticle to acquire compounds of environmental origin. We then tested whether individuals acquire hydrocarbons from the environment, and whether this capability equally characterises newly emerged and mature wasps. We exposed wasps of two age classes (adults younger or older than 24 h) to four linear hydrocarbons in turn, and observed how nestmates reacted to their re-introduction into the natal colony. Exposed young wasps elicited significantly more aggressive responses than control sisters; but treated wasps older than 24 h were generally accepted by nestmates. Chemical assays showed that exposed young wasps readily absorbed hydrocarbons; older ones did not incorporate hydrocarbons, suggesting that the chemical profiles of mature wasps are less prone to chemical shifts than those of newly emerged wasps.     

Assembly and breakdown of Cajal bodies in accessory nuclei of Hymenoptera

In some species of insects, oocytes have vesicular organelles, termed accessory nuclei (ANs). The ANs form by budding off from the nuclear envelope of the oocyte and are filled with translucent matrix containing dense inclusions. One type of these inclusions contains coilin and small nuclear ribonucleoproteins (snRNPs) and is homologous to Cajal bodies. We describe the early events in the morphogenesis of Cajal bodies in the ANs (ANCBs) of the common wasp, Vespula germanica, and show that they contain survival of motor neurons (SMN) protein. We present evidence that in the wasp, ANCBs form by the gradual accumulation of aggregates composed of SMN and small nuclear RNAs. We also show that ANCBs break down and disperse within the ANs as the ANs, which initially surround the oocyte nucleus, localize to the oocyte cortex. The components of dispersed ANCBs are retained within ANs until the end of oogenesis, which suggests that their function may be required at the onset of embryonic development. Because the morphology and behavior of ANs and their Cajal body-like inclusions are conserved in two other hymenopteran species, these features might be characteristic of all hymenopterans.     

寄生蜂核型特征及其在分类上的应用

回顾了寄生性膜翅目昆虫（寄生蜂）染色体数目和核型的研究情况及其在寄生蜂分类中的应用,并对寄生蜂核型分类的前景作了讨论。核型对众多的寄生性膜翅目类群来说可以提供许多分类上的信息,并在种类研究上作用最为显著。通过核型数据的进一步积累和染色体显带方法的进一步应用,寄生蜂的核型分类学将得到进一步的发展。