Partitioning of herbivore hosts across time and food plants promotes diversification in the Megastigmus dorsalis oak gall parasitoid complex

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.

Mechanisms structuring host–parasitoid networks in a global warming context: a review

“…Shifts in the geographical distribution of species' ranges are a common response to global warming: populations colonise new localities and habitats as these become thermally suitable, while retreating from regions and habitats that become too hot (Jeffs & Lewis, 2013;Nicholls et al, 2018). For a Drosophila-parasitoid system, Davis et al (1998b) demonstrated using microcosm experiments that range shifts depend not only on temperatures but also on species interactions and the effect of temperature on them.…”

Habitat or temporal isolation: Unraveling herbivore–parasitoid speciation patterns using double digest RADseq

“…HAD has been recorded in diverse insect families across multiple orders (Antwi, Sword, & Medina, ; Ferrari, West, Via, & Godfray, ; Leppanen, Malm, Varri, & Nyman, ; Sword, Joern, & Senior, ), further suggesting that it is an important driver of speciation that contributed to the insect biodiversity we see today. In addition, HAD can have rippling effects at higher trophic levels, resulting in divergence of parasitoids in the form of cascading/sequential HAD (Abrahamson & Weis, ; Forbes, Powell, Stelinski, Smith, & Feder, ; Hood et al., ; Nicholls, Schönrogge, Preuss, & Stone, ; Stireman, Nason, Heard, & Seehawer, ). As many parasitoids are also cryptic specialists that are tightly linked to the phenology of their hosts, cascading HAD on species lineages of herbivores could result in the sequential radiation of these hyperdiverse lineages of parasitoids (Forbes et al., ; Hood et al., ; Stireman et al., ).…”

“…As many parasitoids are also cryptic specialists that are tightly linked to the phenology of their hosts, cascading HAD on species lineages of herbivores could result in the sequential radiation of these hyperdiverse lineages of parasitoids (Forbes et al., ; Hood et al., ; Stireman et al., ). However, many previous studies of HAD and sequential HAD were limited to few molecular markers (Antwi et al., ; Hood et al., ; Leppanen et al., ; Nicholls et al., ; Stireman et al., ), which provides limited molecular characters to examine fine‐scaled species‐level differentiation. In addition, most studies focus on specialist herbivores with few studies on parasitoids.…”

“…In addition, most studies focus on specialist herbivores with few studies on parasitoids. Studies that have involved examinations of parasitoids have mainly included assemblages of distantly related parasitoids that make inferences about drivers of diversification in upper trophic levels difficult (Hood et al., ; Nicholls et al., ; Stireman et al., ). Therefore, studies focusing on closely related parasitoids species are needed to examine patterns of speciation due to ecologically divergent selection.…”

“…In addition, HAD can have rippling effects at higher trophic levels, resulting in divergence of parasitoids in the form of cascading/sequential HAD (Abrahamson & Weis, 1997;Forbes, Powell, Stelinski, Smith, & Feder, 2009;Hood et al, 2015;Nicholls, Schönrogge, Preuss, & Stone, 2018;Stireman, Nason, Heard, & Seehawer, 2006). As many parasitoids are also cryptic specialists that are tightly linked to the phenology of their hosts, cascading HAD on species lineages of herbivores could result in the sequential radiation of these hyperdiverse lineages of parasitoids (Forbes et al, 2009;Hood et al, 2015;Stireman et al, 2006).…”