The final frontier: ecological and evolutionary dynamics of a global parasite invasion.

Studying rapid biological changes accompanying the introduction of alien organisms into native ecosystems can provide insights into fundamental ecological and evolutionary theory. While powerful, this quasi-experimental approach is difficult to implement because the timing of invasions and their consequences are hard to predict, meaning that baseline pre-invasion data are often missing. Exceptionally, the eventual arrival of Varroa destructor (hereafter Varroa) in Australia has been predicted for decades. Varroa is a major driver of honeybee declines worldwide, particularly as vectors of diverse RNA viruses. The detection of Varroa in 2022 at over a hundred sites poses a risk of further spread across the continent. At the same time, careful study of Varroa's spread, if it does become established, can provide a wealth of information that can fill knowledge gaps about its effects worldwide. This includes how Varroa affects honeybee populations and pollination. Even more generally, Varroa invasion can serve as a model for evolution, virology and ecological interactions between the parasite, the host and other organisms.

Genetic Diversity in the Progeny of Commercial Australian Queen Honey Bees (Hymenoptera: Apidae) Produced in Autumn and Early Spring.

Honey bee [Apis mellifera L. (Hymenoptera: Apidae)] queens are polyandrous, mating with an average 12 males (drones). Polyandry has been shown to confer benefits to queens and the colonies they head, including avoidance of inviable brood that can arise via sex locus homozygosity, increased resilience to pests and pathogens, and increased survival and productivity, leading to improved colony-level fitness. Queens with an effective mating frequency (ke) greater than 7 are considered adequately mated, whereas queens that fall below this threshold head colonies that have increased likelihood of failure and may be less productive for beekeepers. We determined ke in queens produced in early Spring and Autumn by five Australian commercial queen producers to determine whether the queens they produced were suitably mated. Drone populations are low at these times of year, and therefore, there is an increased risk that queens would fall below the ke > 7 threshold. We found that 33.8% of Autumn-produced queens did not meet the threshold, whereas 93.8% of Spring queens were adequately mated. The number of colonies contributing drones to the mating pool was similarly high in both seasons, suggesting that although many colonies have drones, their numbers may be decreased in Autumn and management strategies may be required to boost drone numbers at this time. Finally, queens had similar levels of homozygosity to workers, and inbreeding coefficients were very low, suggesting that inbreeding is not a problem.

Strikingly high levels of heterozygosity despite 20 years of inbreeding in a clonal honey bee.

Inbreeding (the mating between closely related individuals) often has detrimental effects that are associated with loss of heterozygosity at overdominant loci, and the expression of deleterious recessive alleles. However, determining which loci are detrimental when homozygous, and the extent of their phenotypic effects, remains poorly understood. Here, we utilize a unique inbred population of clonal (thelytokous) honey bees, Apis mellifera capensis, to determine which loci reduce individual fitness when homozygous. This asexual population arose from a single worker ancestor approximately 20 years ago and has persisted for at least 100 generations. Thelytokous parthenogenesis results in a 1/3 of loss of heterozygosity with each generation. Yet, this population retains heterozygosity throughout its genome due to selection against homozygotes. Deep sequencing of one bee from each of the three known sub-lineages of the population revealed that 3,766 of 10,884 genes (34%) have retained heterozygosity across all sub-lineages, suggesting that these genes have heterozygote advantage. The maintenance of heterozygosity in the same genes and genomic regions in all three sub-lineages suggests that nearly every chromosome carries genes that show sufficient heterozygote advantage to be selectively detrimental when homozygous.

Subfamily-dependent alternative reproductive strategies in worker honeybees.

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.

The complexity of mating decisions in stalk-eyed flies.

All too often, studies of sexual selection focus exclusively on the responses in one sex, on single traits, typically those that are exaggerated and strongly sexually dimorphic. They ignore a range of less obvious traits and behavior, in both sexes, involved in the interactions leading to mate choice. To remedy this imbalance, we analyze a textbook example of sexual selection in the stalk-eyed fly (Diasemopsis meigenii). We studied several traits in a novel, insightful, and efficient experimental design, examining 2,400 male-female pairs in a "round-robin" array, where each female was tested against multiple males and vice versa. In D. meigenii, females exhibit strong mate preference for males with highly exaggerated eyespan, and so we deliberately constrained variation in male eyespan to reveal the importance of other traits. Males performing more precopulatory behavior were more likely to attempt to mate with females and be accepted by them. However, behavior was not a necessary part of courtship, as it was absent from over almost half the interactions. Males with larger reproductive organs (testes and accessory glands) did not make more mating attempts, but there was a strong tendency for females to accept mating attempts from such males. How females detect differences in male reproductive organ size remains unclear. In addition, females with larger eyespan, an indicator of size and fecundity, attracted more mating attempts from males, but this trait did not alter female acceptance. Genetic variation among males had a strong influence on male mating attempts and female acceptance, both via the traits we studied and other unmeasured attributes. These findings demonstrate the importance of assaying multiple traits in males and females, rather than focusing solely on prominent and exaggerated sexually dimorphic traits. The approach allows a more complete understanding of the complex mating decisions made by both males and females.

A SNP test to identify Africanized honeybees via proportion of 'African' ancestry.

The honeybee, Apis mellifera, is the world's most important pollinator and is ubiquitous in most agricultural ecosystems. Four major evolutionary lineages and at least 24 subspecies are recognized. Commercial populations are mainly derived from subspecies originating in Europe (75-95%). The Africanized honeybee is a New World hybrid of A. m. scutellata from Africa and European subspecies, with the African component making up 50-90% of the genome. Africanized honeybees are considered undesirable for bee-keeping in most countries, due to their extreme defensiveness and poor honey production. The international trade in honeybees is restricted, due in part to bans on the importation of queens (and semen) from countries where Africanized honeybees are extant. Some desirable strains from the United States of America that have been bred for traits such as resistance to the mite Varroa destructor are unfortunately excluded from export to countries such as Australia due to the presence of Africanized honeybees in the USA. This study shows that a panel of 95 single nucleotide polymorphisms, chosen to differentiate between the African, Eastern European and Western European lineages, can detect Africanized honeybees with a high degree of confidence via ancestry assignment. Our panel therefore offers a valuable tool to mitigate the risks of spreading Africanized honeybees across the globe and may enable the resumption of queen and bee semen imports from the Americas.

Population genetics of commercial and feral honey bees in Western Australia.

Due to the introduction of exotic honey bee (Apis mellifera L.) diseases in the eastern states, the borders of the state of Western Australia were closed to the import of bees for breeding and other purposes > 25 yr ago. To provide genetically improved stock for the industry, a closed population breeding program was established that now provides stock for the majority of Western Australian beekeepers. Given concerns that inbreeding may have resulted from the closed population breeding structure, we assessed the genetic diversity within and between the breeding lines by using microsatellite and mitochondrial markers. We found that the breeding population still maintains considerable genetic diversity, despite 25 yr of selective breeding. We also investigated the genetic distance of the closed population breeding program to that of beekeepers outside of the program, and the feral Western Australian honey bee population. The feral population is genetically distinct from the closed population, but not from the genetic stock maintained by beekeepers outside of the program. The honey bees of Western Australia show three mitotypes, originating from two subspecies: Apis mellifera ligustica (mitotypes C1 and M7b) and Apis mellifera iberica (mitotype M6). Only mitotypes C1 and M6 are present in the commercial populations. The feral population contains all three mitotypes.

Entomology: Asian honeybees parasitize the future dead.

The queen of a honeybee colony has a reproductive monopoly because her workers' ovaries are normally inactive and any eggs that they do lay are eaten by their fellow workers. But if a colony becomes queenless, the workers start to lay eggs, stop policing and rear a last batch of males before the colony finally dies out. Here we show that workers of the Asian dwarf red honeybee Apis florea from other colonies exploit this interval as an opportunity to move in and lay their own eggs while no policing is in force. Such parasitism of queenless colonies does not occur in the western honeybee A. mellifera and may be facilitated by the accessibility of A. florea nests, which are built out in the open.