An official website of the United States government
ABSTRACT For insects known as parasitoid wasps, successful development as a parasite results in the death of the host insect. As a result of this lethal interaction, wasps and their hosts have coevolved strategies to gain an advantage in this evolutionary arms race. Although normally considered to be strict pathogens, some viruses have established persistent infections within parasitoid wasp lineages and are beneficial to wasps during parasitism. Heritable associations between viruses and parasitoid wasps have evolved independently multiple times, but most of these systems remain largely understudied with respect to viral origin, transmission and replication strategies of the virus, and interactions between the virus and host insects. Here, we report a detailed characterization of Diachasmimorpha longicaudata entomopoxvirus (DlEPV), a poxvirus found within the venom gland of Diachasmimorpha longicaudata wasps. Our results show that DlEPV exhibits similar but distinct transmission and replication dynamics compared to those of other parasitoid viral elements, including vertical transmission of the virus within wasps, as well as virus replication in both female wasps and fruit fly hosts. Functional assays demonstrate that DlEPV is highly virulent within fly hosts, and wasps without DlEPV have severely reduced parasitism success compared to those with a typical viral load. Taken together, the data presented in this study illustrate a novel case of beneficial virus evolution, in which a virus of unique origin has undergone convergent evolution with other viral elements associated with parasitoid wasps to provide an analogous function throughout parasitism. IMPORTANCE Viruses are generally considered to be disease-causing agents, but several instances of beneficial viral elements have been identified in insects called parasitoid wasps. These virus-derived entities are passed on through wasp generations and enhance the success of the wasps’ parasitic life cycle. Many parasitoid-virus partnerships studied to date exhibit common features among independent cases of this phenomenon, including a mother-to-offspring route of virus transmission, a restricted time and location for virus replication, and a positive effect of virus activity on wasp survival. Our characterization of Diachasmimorpha longicaudata entomopoxvirus (DlEPV), a poxvirus found in Diachasmimorpha longicaudata parasitoid wasps, represents a novel example of beneficial virus evolution. Here, we show that DlEPV exhibits functional similarities to known parasitoid viral elements that support its comparable role during parasitism. Our results also demonstrate unique differences that suggest DlEPV is more autonomous than other long-term viral associations described in parasitoid wasps.
more »
« less
A host driven parasitoid syndrome: Convergent evolution of multiple traits associated with woodboring hosts in Ichneumonidae (Hymenoptera, Ichneumonoidea)
The evolution of convergent phenotypes is of major interest in biology because of their omnipresence and ability to inform the study of evolutionary novelty and constraint. Convergent phenotypes can be combinations of traits that evolve concertedly, called syndromes, and these can be shaped by a common environmental pressure. Parasitoid wasps which use a wide variety of arthropod hosts have also repeatedly and convergently switched host use across their evolutionary history. They thus represent a natural laboratory for the evolution of trait syndromes that are associated with parasitism of specific hosts and host substrates. In this study, we tested the evolution of co-evolving characters in the highly diverse family Ichneumonidae associated with ovipositing in a specific and well-defined substrate: wood. Using a newly constructed phylogeny and an existing morphological dataset, we identified six traits correlated with the wood-boring lifestyle that demonstrate convergent evolution. At least one trait, the presence of teeth on the ovipositor, typically preceded the evolution of other traits and possibly the switch to parasitism of wood-boring hosts. For each trait, we provide a historical review of their associations with wood-boring parasitoids, reevaluate the function of some characters, and suggest future coding improvements. Overall, we demonstrate the convergent evolution of multiple traits associated with parasitism of woodboring hosts and propose a syndrome in a hyper diverse lineage of parasitoid wasps.
more »
« less
- Award ID(s):
- 1916914
- PAR ID:
- 10654630
- Editor(s):
- Khan, Salman
- Publisher / Repository:
- Public Library of Science One
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 19
- Issue:
- 9
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0311365
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Social parasites exploit the brood care behavior of their hosts to raise their own offspring. Social parasites are common among eusocial Hymenoptera and exhibit a wide range of distinct life history traits in ants, bees, and wasps. In ants, obligate inquiline social parasites are workerless (or nearly-so) species that engage in lifelong interactions with their hosts, taking advantage of the existing host worker forces to reproduce and exploit host colonies’ resources. Inquiline social parasites are phylogenetically diverse with approximately 100 known species that evolved at least 40 times independently in ants. Importantly, ant inquilines tend to be closely related to their hosts, an observation referred to as ‘Emery’s Rule’. Polygyny, the presence of multiple egg-laying queens, was repeatedly suggested to be associated with the origin of inquiline social parasitism, either by providing the opportunity for reproductive cheating, thereby facilitating the origin of social parasite species, and/or by making polygynous species more vulnerable to social parasitism via the acceptance of additional egg-laying queens in their colonies. Although the association between host polygyny and the evolution of social parasitism has been repeatedly discussed in the literature, it has not been statistically tested in a phylogenetic framework across the ants. Here, we conduct a meta-analysis of ant social structure and social parasitism, testing for an association between polygyny and inquiline social parasitism with a phylogenetic correction for independent evolutionary events. We find an imperfect but significant over-representation of polygynous species among hosts of inquiline social parasites, suggesting that while polygyny is not required for the maintenance of inquiline social parasitism, it (or factors associated with it) may favor the origin of socially parasitic behavior. Our results are consistent with an intra-specific origin model for the evolution of inquiline social parasites by sympatric speciation but cannot exclude the alternative, inter-specific allopatric speciation model. The diversity of social parasite behaviors and host colony structures further supports the notion that inquiline social parasites evolved in parallel across unrelated ant genera in the formicoid clade via independent evolutionary pathways.more » « less
-
Roossinck, Marilyn J. (Ed.)Insects are known to host a wide variety of beneficial microbes that are fundamental to many aspects of their biology and have substantially shaped their evolution. Notably, parasitoid wasps have repeatedly evolved beneficial associations with viruses that enable developing wasps to survive as parasites that feed from other insects. Ongoing genomic sequencing efforts have revealed that most of these virus-derived entities are fully integrated into the genomes of parasitoid wasp lineages, representing endogenous viral elements (EVEs) that retain the ability to produce virus or virus-like particles within wasp reproductive tissues. All documented parasitoid EVEs have undergone similar genomic rearrangements compared to their viral ancestors characterized by viral genes scattered across wasp genomes and specific viral gene losses. The recurrent presence of viral endogenization and genomic reorganization in beneficial virus systems identified to date suggest that these features are crucial to forming heritable alliances between parasitoid wasps and viruses. Here, our genomic characterization of a mutualistic poxvirus associated with the wasp Diachasmimorpha longicaudata , known as Diachasmimorpha longicaudata entomopoxvirus (DlEPV), has uncovered the first instance of beneficial virus evolution that does not conform to the genomic architecture shared by parasitoid EVEs with which it displays evolutionary convergence. Rather, DlEPV retains the exogenous viral genome of its poxvirus ancestor and the majority of conserved poxvirus core genes. Additional comparative analyses indicate that DlEPV is related to a fly pathogen and contains a novel gene expansion that may be adaptive to its symbiotic role. Finally, differential expression analysis during virus replication in wasps and fly hosts demonstrates a unique mechanism of functional partitioning that allows DlEPV to persist within and provide benefit to its parasitoid wasp host.more » « less
-
ABSTRACT Extreme high temperatures associated with climate change can affect species directly, and indirectly through temperature-mediated species interactions. In most host–parasitoid systems, parasitization inevitably kills the host, but differences in heat tolerance between host and parasitoid, and between different hosts, may alter their interactions. Here, we explored the effects of extreme high temperatures on the ecological outcomes – including, in some rare cases, escape from the developmental disruption of parasitism – of the parasitoid wasp, Cotesia congregata, and two co-occurring congeneric larval hosts, Manduca sexta and M. quinquemaculata. Both host species had higher thermal tolerance than C. congregata, resulting in a thermal mismatch characterized by parasitoid (but not host) mortality under extreme high temperatures. Despite parasitoid death at high temperatures, hosts typically remain developmentally disrupted from parasitism. However, high temperatures resulted in a partial developmental recovery from parasitism (reaching the wandering stage at the end of host larval development) in some host individuals, with a significantly higher frequency of this partial developmental recovery in M. quinquemaculata than in M. sexta. Hosts species also differed in their growth and development in the absence of parasitoids, with M. quinquemaculata developing faster and larger at high temperatures relative to M. sexta. Our results demonstrate that co-occurring congeneric species, despite shared environments and phylogenetic histories, can vary in their responses to temperature, parasitism and their interaction, resulting in altered ecological outcomes.more » « less
-
When ecological and evolutionary dynamics occur on comparable timescales, persistence of the ensuing eco-evolutionary dynamics requires both ecological and evolutionary stability. This unites key questions in ecology and evolution: How do species coexist, and what maintains genetic variation in a population? In this work, we investigated a host-parasitoid system in which pea aphid hosts rapidly evolve resistance toAphidius erviparasitoids. Field data and mathematical simulations showed that heterogeneity in parasitoid dispersal can generate variation in parasitism-mediated selection on hosts through time and space. Experiments showed how evolutionary trade-offs plus moderate host dispersal across this selection mosaic cause host-parasitoid coexistence and maintenance of genetic variation in host resistance. Our results show how dispersal can stabilize both the ecological and evolutionary components of eco-evolutionary dynamics.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pone.0311365
