Abstract
Communities of insect herbivores and their natural enemies are rich and ecologically crucial components of terrestrial biodiversity. Understanding the processes that promote their origin and maintenance is thus of considerable interest. One major proposed mechanism is ecological speciation through host‐associated differentiation (HAD), the divergence of a polyphagous species first into ecological host races and eventually into more specialized daughter species. The rich chalcid parasitoid communities attacking cynipid oak gall wasp hosts are structured by multiple host traits, including food plant taxon, host gall phenology, and gall structure. Here, we ask whether the same traits structure genetic diversity within supposedly generalist parasitoid morphospecies. We use mitochondrial DNA sequences and microsatellite genotypes to quantify HAD for Megastigmus (Bootanomyia) dorsalis, a complex of two apparently generalist cryptic parasitoid species attacking oak galls. Ancient Balkan refugial populations showed phenological separation between the cryptic species, one primarily attacking spring galls, and the other mainly attacking autumn galls. The spring species also contained host races specializing on galls developing on different host‐plant lineages (sections Cerris vs. Quercus) within the oak genus Quercus. These results indicate more significant host‐associated structuring within oak gall parasitoid communities than previously thought and support ecological theory predicting the evolution of specialist lineages within generalist parasitoids. In contrast, UK populations of the autumn cryptic species associated with both native and recently invading oak gall wasps showed no evidence of population differentiation, implying rapid recruitment of native parasitoid populations onto invading hosts, and hence potential for natural biological control. This is of significance given recent rapid range expansion of the economically damaging chestnut gall wasp, Dryocosmus kuriphilus, in Europe.
Highlights
Insect communities comprising insect herbivores and their parasitoid natural enemies dominate terrestrial animal biodiversity and fulfill multiple ecological roles (Feder & Forbes, 2010; Futuyma & Agrawal, 2009; May, 1990; Santos & Quicke, 2011)
Work in a growing number of systems shows that insect herbivore morphospecies often harbor genetically diverging lineages, termed ecological host races or biotypes, that specialize on a subset of the full host-plant range (Abrahamson, Blair, Eubanks, & Morehead, 2003; Drès & Mallet, 2002; Linn et al, 2003; Lozier, Roderick, & Mills, 2007; Powell, Forbes, Hood, & Feder, 2014)
The paradox is that we expect generalist parasitoids to reduce host species richness because, in the absence of other structuring processes, parasitoid populations that result from attack of one host can have negative impacts on other hosts and potentially drive these to extinction, a process termed apparent competition (Holt & Lawton, 1993; Morris, Lewis, & Godfray, 2004; Stone & Schönrogge, 2003)
Summary
Insect communities comprising insect herbivores and their parasitoid natural enemies dominate terrestrial animal biodiversity and fulfill multiple ecological roles (Feder & Forbes, 2010; Futuyma & Agrawal, 2009; May, 1990; Santos & Quicke, 2011). Host-associated differentiation within parasitoid taxa is of particular interest because it could resolve an apparent paradox present in many communities comprising specific guilds of insect herbivores (such as leaf miners or gall inducers) and their parasitoid natural enemies Such communities often combine both high species richness of herbivore hosts, and large numbers of generalist parasitoids (those attacking a wide host range). High herbivore host diversity and shared generalist natural enemies can be reconciled if apparent generalist enemies comprise genetically divergent cryptic lineages that each attack only a subset of the species’ recorded host range Such structuring has been revealed in a range of systems (Forbes, Powell, Stelinski, Smith, & Feder, 2009; Hood et al, 2015; Smith, Wood, Janzen, Hallwachs, & Hebert, 2007; Smith et al, 2008; Stireman et al, 2006). Understanding how insect herbivores and parasitoid communities are structured has implications for many aspects of ecosystem management, including biological control of herbivorous pests (Carvalheiro, Buckley, Ventim, Fowler, & Memmott, 2008; Henneman & Memmott, 2001), and predicting the impacts of range expansions associated with anthropogenic introductions and climate change (Nicholls, Fuentes- Utrilla, et al, 2010; Sax et al, 2007)
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