Population genomics of the invasive Northern Giant Hornet Vespa mandarinia in North America and across its native range.

The northern giant hornet Vespa mandarinia (NGH) is a voracious predator of other insect species, including honey bees. NGH's native range spans subtropical and temperate regions across much of east and southeast Asia and, in 2019, exotic populations of the species were discovered in North America. Despite this broad range and invasive potential, investigation of the population genomic structure of NGH across its native and introduced ranges has thus far been limited to a small number of mitochondrial samples. Here, we present analyses of genomic data from NGH individuals collected across the species' native range and from exotic individuals collected in North America. We provide the first survey of whole-genome population variation for any hornet species, covering this species' native and invasive ranges, and in doing so confirm likely origins in Japan and South Korea for the two introductions. We additionally show that, while this introduced population exhibited strongly elevated levels of inbreeding, these signatures of inbreeding are also present in some long-standing native populations, which may indicate that inbreeding depression alone is insufficient to prevent the persistence of NGH populations. As well as highlighting the importance of ongoing monitoring and eradication efforts to limit the spread of this species outside of its natural range, our data will serve as a foundational database for future genomic studies into introduced hornet populations.

Unequal Reproduction Early in a Social Transition: Insights from Invasive Wasps.

AbstractIn eusocial insects, nestmate queens can differ in their reproductive output, causing asymmetries in the distribution of mutual benefits. However, little is known about how reproductive success is partitioned in incipiently polygynous species, which would provide clues about the evolutionary forces shaping the emergence of polygyny. Here, we leverage a recent transition from predominantly single-queen (monogyne) to multiple-queen (polygyne) colonies in an invasive yellowjacket species to investigate whether queens in incipiently polygyne colonies invest equally in reproductive effort or vary in their relative investment in each caste. We excavated nine polygyne Vespula pensylvanica colonies in Hawaii and used restriction site-associated DNA sequencing to infer the parentage of worker, male, and gyne (daughter queen) pupae from each nest comb. In four colonies with at least eight gyne pupae, a single queen produced most or all gynes. These queens had no male offspring and few worker offspring, suggesting that a subset of nestmate queens might exploit the collective benefits of newly polygyne societies. In contrast to most queens, gyne producers had offspring distributed nonrandomly across nest combs. Nestmate queens generally exhibited low relatedness levels. Our results suggest that rapid, ecologically driven transitions to polygyny among unrelated queens may, at their onset, be vulnerable to reproductive asymmetries that are likely evolutionarily unstable. More broadly, this study contributes to the understanding of social evolution by uncovering asymmetric partitioning of reproduction in a population with newly evolved polygyny and raises questions about the future trajectories of introduced populations.

A novel distribution of supergene genotypes is present in the socially polymorphic ant Formica neoclara.

BACKGROUND: Supergenes are chromosomal regions with tightly linked clusters of alleles that control compound phenotypic traits. Supergenes have been demonstrated to contribute to the maintenance of polymorphisms within populations in traits as diverse as mimetic wing coloration in butterflies, mating strategies in birds, and malarial susceptibility in mosquitoes. A large supergene also underlies variation in social organization in Formica ants. Alternative supergene haplotypes are associated with the presence of either a single queen (monogyny) or multiple queens (polygyny) within colonies. Here, we assess the social structure and supergene status of the North American species Formica neoclara. RESULTS: We sequenced a subset of the genome in 280 individuals sampled in populations from California to northern British Columbia using ddRADseq. We determined that F. neoclara is socially polymorphic in queen number, and we show that the social polymorphism is associated with alternative haplotypes at the social supergene. Intriguingly, polygyne colonies can harbor workers that are homozygous for both haplotypes as well as heterozygotes. CONCLUSIONS: This colony genetic composition contrasts with other Formica species, in which almost all individuals in polygyne colonies have the polygyne-associated haplotype. The social polymorphism is present in widely distributed and genetically subdivided populations of F. neoclara. In studying this system in F. neoclara, we expand our understanding of the functional evolution of supergene haplotypes as they diverge in different lineages.

Early queen joining and long-term queen associations in polygyne colonies of an invasive wasp revealed by longitudinal genetic analysis.

Invasive social insects rank among the most damaging of terrestrial species. They are responsible for extensive damage and severely threaten the biodiversity of environments where they are introduced. Variation in colony social form commonly occurs in introduced populations of yellowjacket wasps (genus Vespula). In particular, invasive colonies may contain multiple queens (i.e., polygyne) and persist several years, while in the native range, the colonies are usually annual and harbor a single queen (i.e., monogyne). In this study, we used genome-wide loci obtained by double digest restriction site-associated DNA sequencing (RADseq) to investigate the genetic structure and queen turnover in colonies of the western yellowjacket, Vespula pensylvanica, in their introduced range in Hawaii. Of the 27 colonies monitored over four months (October-January), 19 were polygyne and already contained multiple queens on the first day of sampling. Contrary to previous speculation, this finding suggests that polygyny often arises early in the annual colony cycle, before the production of new queens in the fall. Furthermore, polygyne colonies exhibited a prolonged average lifespan relative to those headed by a single queen. As a result, there is no clear window during which colony eradication efforts would be more effective than upon first discovery. The relatedness among nestmate queens was slightly above zero, indicating that these colonies are generally composed of nonrelatives. The queen turnover within each colony was low, and we detected some full-sibling workers sampled up to four months apart. Finally, we did not detect any population structure among colonies, suggesting that queens disperse up to several kilometers. Taken together, our results provide the first insights into the requeening dynamics in this invasive and incipiently polygyne population and illuminate the early establishment of multiple long-lasting queens in these damaging colonies.

Ant nest architecture is shaped by local adaptation and plastic response to temperature.

Social insects are among the most abundant arthropods in terrestrial ecosystems, where they provide ecosystem services. The effect of subterranean activity of ants on soil is well-studied, yet little is known about nest architecture due to the difficulty of observing belowground patterns. Furthermore, many species' ranges span environmental gradients, and their nest architecture is likely shaped by the climatic and landscape features of their specific habitats. We investigated the effects of two temperature treatments on the shape and size of nests built by Formica podzolica ants collected from high and low elevations in the Colorado Rocky Mountains in a full factorial experiment. Ants nested in experimental chambers with soil surface temperatures matching the local temperatures of sample sites. We observed a plastic response of nest architecture to conditions experienced during excavation; workers experiencing a high temperature excavated deeper nests than those experiencing a cooler temperature. Further, we found evidence of local adaptation to temperature, with a significant interaction effect of natal elevation and temperature treatment on nest size and complexity. Specifically, workers from high elevation sites built larger nests with more tunnels when placed in the cool surface temperature treatment, and workers from low elevation sites exhibited the opposite pattern. Our results suggest that subterranean ant nest architecture is shaped by a combination of plastic and locally adapted building behaviors; we suggest that the flexibility of this 'extended phenotype' likely contributes to the widespread success of ants.