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Comprehensive phylogenomic analyses re-write the evolution of parasitism within cynipoid wasps
Background Parasitoidism, a specialized life strategy in which a parasite eventually kills its host, is frequently found within the insect order Hymenoptera (wasps, ants and bees). A parasitoid lifestyle is one of two dominant life strategies within the hymenopteran superfamily Cynipoidea, with the other being an unusual plant-feeding behavior known as galling. Less commonly cynipoid wasps exhibit inquilinism, a strategy where some species have adapted to usurp other species' galls instead of inducing their own. Using a phylogenomic data set of ultraconserved elements from nearly all lineages of Cynipoidea, we here generate a robust phylogenetic framework and timescale to understand cynipoid systematics and the evolution of these life histories. Results Our reconstructed evolutionary history for Cynipoidea differs considerably from previous hypotheses. Rooting our analyses with non-cynipoid outgroups, the Paralaucini, a group of inquilines, emerged as sister-group to the rest of Cynipoidea, rendering the gall wasp family Cynipidae paraphyletic. The families Ibaliidae and Liopteridae, long considered archaic and early-branching parasitoid lineages, were found nested well within the Cynipoidea as sister-group to the parasitoid Figitidae. Cynipoidea originated in the early Jurassic around 190 Ma. Either inquilinism or parasitoidism is suggested as the ancestral and dominant strategy throughout the early evolution of cynipoids, depending on whether a simple (three states: parasitoidism, inquilinism and galling) or more complex (seven states: parasitoidism, inquilinism and galling split by host use) model is employed. Conclusions Our study has significant impact on understanding cynipoid evolution and highlights the importance of adequate outgroup sampling. We discuss the evolutionary timescale of the superfamily in relation to their insect hosts and host plants, and outline how phytophagous galling behavior may have evolved from entomophagous, parasitoid cynipoids. We hypothesize these seemingly diverging life strategies may be considered as specializations of a similar underlying molecular toolkit between which switches are possible. Our study has established the framework for further physiological and comparative genomic work between gall-making, inquiline and parasitoid lineages, which could also have significant implications for the evolution of diverse life histories in other Hymenoptera.
Data from: Niche differentiation and colonization of a novel environment by an asexual parasitic wasp.
How do asexual taxa become adapted to a diversity of environments, and how do they persist despite changing environmental conditions? These questions are linked by their mutual focus on the relationship between genetic variation, which is often limited in asexuals, and the ability to respond to environmental variation. Asexual taxa originating from a single ancestor present a unique opportunity to assess rates of phenotypic and genetic change when access to new genetic variation is limited to mutation. Diachasma muliebre is an asexual Hymenopteran wasp that is geographically and genetically isolated from all sexual relatives. D. muliebre attack larvae of the western cherry fruit fly (Rhagoletis indifferens), which in turn feed inside bitter cherry fruit (Prunus emarginata) in August and September. R. indifferens has recently colonized a new host plant with an earlier fruiting phenology (June/July), domesticated sweet cherries (P. avium), and D. muliebre has followed its host into this temporally earlier niche. We tested three hypotheses: 1) that all D. muliebre lineages originate from a single asexual ancestor; 2) that different D. muliebre lineages (as defined by unique mtDNA haplotypes) have differentiated on their ancestral host in an important life-history trait, eclosion timing; and 3) that early-eclosing lineages have preferentially colonized the new sweet cherry niche. We find that mitochondrial COI and microsatellite data provide strong support for a single ancestral origin for all lineages. Furthermore, COI sequencing revealed five mitochondrial haplotypes among D. muliebre, and individual wasps possessing one distinctive mitochondrial haplotype (haplotype II) eclosed as reproductive adults significantly earlier than wasps with all other haplotypes. In addition, this early-eclosing lineage of D. muliebre is one of two lineages that have colonized the P. avium habitat, consistent with the preferential colonization hypothesis. These data suggest that D. muliebre has evolved adaptive phenotypic variation despite limited genetic variation, and that this variation has subsequently allowed an expansion of some wasps into a novel habitat. The D. muliebre system may allow for in-depth study of adaptation and long-term persistence of asexual taxa.
Data from: Nest signature changes throughout colony cycle and after social parasite invasion in social wasps
Social insects recognize their nestmates by means of a cuticular hydrocarbon signature shared by colony members, but how nest signature changes across time has been rarely tested in longitudinal studies and in the field. In social wasps, the chemical signature is also deposited on the nest surface, where it is used by newly emerged wasps as a reference to learn their colony odor. Here, we investigate the temporal variations of the chemical signature that wasps have deposited on their nests. We followed the fate of the colonies of the social paper wasp Polistes biglumis in their natural environment from colony foundation to decline. Because some colonies were invaded by the social parasite Polistes atrimandibularis, we also tested the effects of social parasites on the nest signature. We observed that, as the season progresses, the nest signature changed; the overall abundance of hydrocarbons as well as the proportion of longer-chain and branched hydrocarbons increased. Where present, social parasites altered the host-nest signature qualitatively (adding parasite-specific alkenes) and quantitatively (by interfering with the increase in overall hydrocarbon abundance). Our results show that 1) colony odor is highly dynamic both in colonies controlled by legitimate foundresses and in those controlled by social parasites; 2) emerged offspring contribute little to colony signature, if at all, in comparison to foundresses; and 3) social parasites, that later mimic host signature, initially mark host nests with species-specific hydrocarbons. This study implies that important updating of the neural template used in nestmate recognition should occur in social insects.
Data from: The geographic structure of selection on a coevolving interaction between social parasitic wasps and their hosts hampers social evolution
Social parasites exploit societies, rather than organisms, and rear their brood in social insect colonies at the expense of their hosts, triggering a coevolutionary process that may affect host social structure. The resulting coevolutionary trajectories may be further altered by selection imposed by predators, which exploit the abundant resources concentrated in these nests. Here, we show that geographic differences in selection imposed by predators affects the structure of selection on coevolving hosts and their social parasites. In a multi-year study, we monitored the fate of the annual breeding attempts of the solitary-founding females of Polistes biglumis social wasps in four geographically distinct populations that varied in levels of attack by the congeneric social parasite, P. atrimandibularis. Foundress fitness depended mostly on whether, during the long founding phase, a colony was invaded by social parasites or attacked by predators. Foundresses from each population differed in morphological traits and reproductive tactics that were consistent with selection imposed by their natural enemies and in ways that may affect host sociality. In turn, parasite traits were consistent with selection imposed locally by hosts, implying a geographic mosaic of coevolution in this brood parasitic interaction.
FIGURES 10–16 in Three new species of the parasitic wasps genus Spilomicrus Westwood (Hymenoptera: Diapriidae) from the East Palaearctic Region
FIGURES 10–16. Spilomicrus nottoni sp. nov., female (10–12, 14–15) and male (13, 16). 10, head, lateral view; 11, 13, whole insect, lateral view; 12, face; 14, mesosoma, dorsal view; 15, whole antenna; 16, antennae (A2–A5); aim, anterior incision of mesopleuron.
FIGURES 1–9 in Three new species of the parasitic wasps genus Spilomicrus Westwood (Hymenoptera: Diapriidae) from the East Palaearctic Region
FIGURES 1–9. Spilomicrus notaulus sp. nov., female (1–2, 6–9) and male (3–5). 1, 4, head, dorsal view; 2, 5, whole insect, lateral view; 3, face; 6, mesosoma, dorsal view; 7, whole antenna; 8, petiole, dorsal view; 9, antenna (A2–A4); DP, pleurostomal distance; WH, width of head.
FIGURES 26–28 in Three new species of the parasitic wasps genus Spilomicrus Westwood (Hymenoptera: Diapriidae) from the East Palaearctic Region
FIGURES 26–28. Spilomicrus stigmaticalis Westwood, female (28) and male (26–27). 26, mesosoma, ventral view; 27 antennae (A2–A5); 28, head, dorsal view.
FIGURES 17–25 in Three new species of the parasitic wasps genus Spilomicrus Westwood (Hymenoptera: Diapriidae) from the East Palaearctic Region
FIGURES 17–25. Spilomicrus lubomasneri sp. nov., female (17–20, 22–25) and male (21). 17, head, lateral view; mesosoma, dorsal view (18) and ventral view (25); 19, petiole, dorsal view; 20, whole insect, lateral view; 21, 22, whole antenna; 23, face; 24, head, frontal view.
FIGURE 7 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 7. Nipponodipogon sudai sp. nov. (A–F, holotype, ♀; G–K, paratype, ♂, Japan). A. head, frontal view; B. head, lateral view; C, G. head, dorsal view; D. mesosoma, lateral view; E. apical portion of left hind femur, outer view; F. S1, ventrolateral view; H. S6, ventrolateral view; I. subgenital plate, lateral view; J. genitalia (left half, dorsal view; right half, ventral view); K. aedeagus and parapenial lobe, dorsal view. Scale lines: 0.5 mm.
FIGURE 6 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 6. Nipponodipogon rossicus. (A–F, holotype, ♀; G–J, paratype, ♂, Russian Far East). A. head, frontal view; B. head, lateral view; C, G. head, dorsal view; D. mesosoma, lateral view; E. T1, dorsal view; F. S1 and S2, ventral view; H. S6, ventral view; I. subgenital plate, lateral view; J. genitalia (left half, dorsal view; right half, ventral view). Scale lines: 0.5 mm.
FIGURE 1 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 1. Nipponodipogon hayachinensis, ♀, type locality. A. head, frontal view; B. head, dorsal view; C. propodeum, lateral view; D. outer claw of left hind tarsus. Scale lines: 0.5 mm.
FIGURE 3 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 3. Nipponodipogon kurilensis, holotype, ♀. A. head, frontal view; B. head, dorsal view; C. mesosoma, lateral view; D. T1, dorsal view; E. S1 and S2, ventrolateral view. Scale lines: 0.5 mm.
FIGURE 2 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 2. Nipponodipogon iwatai. (A–E, holotype, ♀; F–I, ♂, Japan). A. head, frontal view; B. head, dorsal view; C. mesosoma, lateral view; D. apical portion of left hind femur, outer view; E. S1 and S2, ventral view; F. S6 and subgenital plate, ventrolateral view; G, subgenital plate, lateral view; H, genitalia, ventral view; I. genitalia, dorsal view. Scale lines: 0.5 mm.
FIGURE 9 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 9. Nipponodipogon, fore and hind wings. A. N. hayachinensis, ♀, Japan; B. N. iwatai, holotype; C, D. N. kurilensis, holotype; E. N. mandibularis, holotype; F, G. N. nagasei, holotype; H, I. N. rossicus, holotype. J. H. sudai sp. nov., paratype, ♀, Japan; K. H. sudai, paratype, ♂, Japan. Scale lines: 1.0 mm.
FIGURE 5 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 5. Nipponodipogon nagasei. (A–D, holotype, ♀; E–G, ♂, Japan). A. head, frontal view; B. head, dorsal view; C. mesosoma, lateral view; D. outer claw of right hind tarsus; E. S6 and subgenital plate, ventrolateral view; F. subgenital plate, lateral view; G. genitalia (left half, ventral view; right half, dorsal view). Scale lines: 0.5 mm.
FIGURE 8 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 8. Nipponodipogon, female head, anterolateral view (A, B), female T1, dorsal view (C–E) and male subgenital plate, ventral view (F–I). A. N. mandibularis, paratype, Japan. B. N. nagasei, Japan. C. N. iwatai, Japan; D. N. nagasei, Japan; E. N. sudai sp. nov., paratype, Japan; F. N. iwatai, Japan; G. N. nagasei, Japan; H. N. rossicus, paratype, Russian Far East; I. N. sudai, paratype, Japan. Scale lines: 0.5 mm for A–E, 0.25 mm for F–I.
FIGURE 4 in Revision of the Palaearctic brood parasitic genus Nipponodipogon Ishikawa, 1965 of spider wasps (Hymenoptera: Pompilidae: Pepsinae)
FIGURE 4. Nipponodipogon mandibularis, holotype, ♀. A. head, frontal view; B. head, dorsal view; C. mesosoma, lateral view. Scale lines: 0.5 mm.
FIGURES 32–37 in Notes on three braconid wasps (Hymenoptera: Braconidae, Doryctinae) parasitizing oak long-horned beetle, Massicus raddei (Coleoptera: Cerambycidae), a severe pest of Quercus spp. in China, together with the description of a new species
FIGURES 32–37. Zombrus bicolor (Enderlein), ♀. 32, Fore leg; 33, fore tibia and spines on it; 34, mid leg; 35, hind leg; 36, fore wing; 37, hind wing. 32–35, lateral view; 36, 37, dorsal view.
FIGURES 5–8. 5 in Notes on three braconid wasps (Hymenoptera: Braconidae, Doryctinae) parasitizing oak long-horned beetle, Massicus raddei (Coleoptera: Cerambycidae), a severe pest of Quercus spp. in China, together with the description of a new species
FIGURES 5–8. 5, young larva of M. raddei under the bark; 6, some of mature larvae of M. raddei from one tree; 7, emergencing of Doryctes petiolatus Shestakov; 8, cocoon of Rhoptrocentrus quercusi sp.n..
FIGURES 22–26 in Notes on three braconid wasps (Hymenoptera: Braconidae, Doryctinae) parasitizing oak long-horned beetle, Massicus raddei (Coleoptera: Cerambycidae), a severe pest of Quercus spp. in China, together with the description of a new species
FIGURES 22–26. Rhoptrocentrus quercusi sp.n., ♀. 22, Head; 23, mesosoma; 24, fore leg; 25, mid leg; 26, hind leg. 22–26, lateral view.
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Allen Brain Atlas
Allen Brain Atlas is an Allen Institute collection of brain map atlases, datasets, APIs, and analysis tools covering mouse, human, and non-human primate brain resources.
Annotated Behaviour and Observability Dataset (ABODe)
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DANDI Archive for NWB datasets
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International Brain Laboratory public data
The International Brain Laboratory public data releases expose standardized mouse decision-making experiments, including Neuropixels recordings, widefield calcium imaging, behavior, and session metadata accessed through the ONE API.
OpenNeuro
OpenNeuro is a free, open platform for sharing neuroimaging datasets, with public search, dataset pages, and download paths for web, S3, DataLad, and the OpenNeuro CLI.