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Unravelling mummies: cryptic diversity, host specificity, trophic and coevolutionary interactions in psyllid - parasitoid food webs.

ABSTRACT: Parasitoids are hyperdiverse and can contain morphologically and functionally cryptic species, making them challenging to study. Parasitoid speciation can arise from specialisation on niches or diverging hosts. However, which process dominates is unclear because cospeciation across multiple parasitoid and host species has rarely been tested. Host specificity and trophic interactions of the parasitoids of psyllids (Hemiptera) remain mostly unknown, but these factors are fundamentally important for understanding of species diversity, and have important applied implications for biological control.We sampled diverse parasitoid communities from eight Eucalyptus-feeding psyllid species in the genera Cardiaspina and Spondyliaspis, and characterised their phylogenetic and trophic relationships using a novel approach that forensically linked emerging parasitoids with the presence of their DNA in post-emergence insect mummies. We also tested whether parasitoids have cospeciated with their psyllid hosts. The parasitoid communities included three Psyllaephagus morphospecies (two primary and, unexpectedly, one heteronomous hyperparasitoid that uses different host species for male and female development), and the hyperparasitoid, Coccidoctonus psyllae. However, the number of genetically delimited Psyllaephagus species was three times higher than the number of recognisable morphospecies, while the hyperparasitoid formed a single generalist species. In spite of this, cophylogenetic analysis revealed unprecedented codivergence of this hyperparasitoid with its primary parasitoid host, suggesting that this single hyperparasitoid species is possibly diverging into host-specific species. Overall, parasitoid and hyperparasitoid diversification was characterised by functional conservation of morphospecies, high host specificity and some host switching between sympatric psyllid hosts.We conclude that host specialisation, host codivergence and host switching are important factors driving the species diversity of endoparasitoid communities of specialist host herbivores. Specialisation in parasitoids can also result in heteronomous life histories that may be more common than appreciated. A host generalist strategy may be rare in endoparasitoids of specialist herbivores despite the high conservation of morphology and trophic roles, and endoparasitoid species richness is likely to be much higher than previously estimated. This also implies that the success of biological control requires detailed investigation to enable accurate identification of parasitoid-host interactions before candidate parasitoid species are selected as biological control agents for target pests.

SUBMITTER: Hall AAG

PROVIDER: S-EPMC5461677 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Unravelling mummies: cryptic diversity, host specificity, trophic and coevolutionary interactions in psyllid - parasitoid food webs.

Hall Aidan A G AAG Steinbauer Martin J MJ Taylor Gary S GS Johnson Scott N SN Cook James M JM Riegler Markus M

BMC evolutionary biology 20170606 1

<h4>Background</h4>Parasitoids are hyperdiverse and can contain morphologically and functionally cryptic species, making them challenging to study. Parasitoid speciation can arise from specialisation on niches or diverging hosts. However, which process dominates is unclear because cospeciation across multiple parasitoid and host species has rarely been tested. Host specificity and trophic interactions of the parasitoids of psyllids (Hemiptera) remain mostly unknown, but these factors are fundame ...[more]

PMID: 28587639

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Project description:Detritivory is the dominant trophic paradigm in most terrestrial, aquatic, and marine ecosystems, yet accurate measurement of consumer trophic position within detrital (="brown") food webs has remained unresolved. Measurement of detritivore trophic position is complicated by the fact that detritus is suffused with microbes, creating a detrital complex of living and nonliving biomass. Given that microbes and metazoans are trophic analogues of each other, animals feeding on detrital complexes are ingesting other detritivores (microbes), which should elevate metazoan trophic position and should be rampant within brown food webs. We tested these hypotheses using isotopic (15N) analyses of amino acids extracted from wild and laboratory-cultured consumers. Vertebrate (fish) and invertebrate detritivores (beetles and moths) were reared on detritus, with and without microbial colonization. In the field, detritivorous animal specimens were collected and analyzed to compare trophic identities among laboratory-reared and free-roaming detritivores. When colonized by bacteria or fungi, the trophic positions of detrital complexes increased significantly over time. The magnitude of trophic inflation was mediated by the extent of microbial consumption of detrital substrates. When detrital complexes were fed to vertebrate and invertebrate animals, the consumers registered similar degrees of trophic inflation, albeit one trophic level higher than their diets. The wild-collected detritivore fauna in our study exhibited significantly elevated trophic positions. Our findings suggest that the trophic positions of detrital complexes rise predictably as microbes convert nonliving organic matter into living microbial biomass. Animals consuming such detrital complexes exhibit similar trophic inflation, directly attributable to the assimilation of microbe-derived amino acids. Our data demonstrate that detritivorous microbes elevate metazoan trophic position, suggesting that detritivory among animals is, functionally, omnivory. By quantifying the impacts of microbivory on the trophic positions of detritivorous animals and then tracking how these effects propagate "up" food chains, we reveal the degree to which microbes influence consumer groups within trophic hierarchies. The trophic inflation observed among our field-collected fauna further suggests that microbial proteins represent an immense contribution to metazoan biomass. Collectively, these findings provide an empirical basis to interpret detritivore trophic identity, and further illuminate the magnitude of microbial contributions to food webs.

Dataset Information

Unravelling mummies: cryptic diversity, host specificity, trophic and coevolutionary interactions in psyllid - parasitoid food webs.

Publications

Unravelling mummies: cryptic diversity, host specificity, trophic and coevolutionary interactions in psyllid - parasitoid food webs.

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