Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes

Abstract

Little is known about the evolutionary history of most complex multi-trophic insect communities. Widespread species from different trophic levels might evolve in parallel, showing similar spatial patterns and either congruent temporal patterns (Contemporary Host-tracking) or later divergence in higher trophic levels (Delayed Host-tracking). Alternatively, host shifts by natural enemies among communities centred on different host resources could disrupt any common community phylogeographic pattern. We examined these alternative models using two Megastigmus parasitoid morphospecies associated with oak cynipid galls sampled throughout their Western Palaearctic distributions. Based on existing host cynipid data, a parallel evolution model predicts that eastern regions of the Western Palaearctic should contain ancestral populations with range expansions across Europe about 1.6 million years ago and deeper species-level divergence at both 8-9 and 4-5 million years ago. Sequence data from mitochondrial cytochrome b and multiple nuclear genes showed similar phylogenetic patterns and revealed cryptic genetic species within both morphospecies, indicating greater diversity in these communities than previously thought. Phylogeographic divergence was apparent in most cryptic species between relatively stable, diverse, putatively ancestral populations in Asia Minor and the Middle East, and genetically depauperate, rapidly expanding populations in Europe, paralleling patterns in host gallwasp species. Mitochondrial and nuclear data also suggested that Europe may have been colonized multiple times from eastern source populations since the late Miocene. Temporal patterns of lineage divergence were congruent within and across trophic levels, supporting the Contemporary Host-tracking Hypothesis for community evolution.

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

“…(2010), 33 of which were shown to be from M. dorsalis sp.1 and two from M. dorsalis sp.2, and a further 281 Hungarian individuals (of which 171 proved to be from M. dorsalis sp.1 and 110 from M. dorsalis sp.2). We generated novel microsatellite data for all 112 M. dorsalis sp.2 individuals.…”

“…Interest in host‐associated differentiation in cynipid galls has grown in response to the detection of morphologically cryptic parasitoid species using molecular approaches (Kaartinen, Stone, Hearn, Lohse, & Roslin, 2010; Nicholls, Preuss, et al., 2010). Several of the parasitoid morphospecies studied by Bailey et al.…”

“…This allows assessment of the impact on genetic structure within a species complex of the same host traits that are known to structure patterns across parasitoid species. Previous molecular analysis of the M. dorsalis complex using sequence data for the mitochondrial cytochrome b gene (cytb) and three unlinked nuclear markers (Nicholls, Preuss, et al., 2010) has shown it to contain two cryptic species (hereafter called M. dorsalis sp.1 and M. dorsalis sp.2), identifiable with 100% accuracy using cytb haplotypes alone. Both cryptic species have distributions that span the Western Palaearctic from the Iberian Peninsula to Iran, and both are also found in northern Europe, including the UK (Nicholls, Preuss, et al., 2010).…”

“…Previous molecular analysis of the M. dorsalis complex using sequence data for the mitochondrial cytochrome b gene (cytb) and three unlinked nuclear markers (Nicholls, Preuss, et al., 2010) has shown it to contain two cryptic species (hereafter called M. dorsalis sp.1 and M. dorsalis sp.2), identifiable with 100% accuracy using cytb haplotypes alone. Both cryptic species have distributions that span the Western Palaearctic from the Iberian Peninsula to Iran, and both are also found in northern Europe, including the UK (Nicholls, Preuss, et al., 2010). Broad overlap in their distributions means that previous host gall wasp records for the morphospecies M. dorsalis cannot be retrospectively assigned either cryptic species on the basis of geography.…”

“…For the second question, we focus on M. dorsalis sp.2 shown by previous work to have high intraspecific genetic diversity (in contrast to M. dorsalis sp.1, which has much less; Nicholls, Preuss, et al., 2010). If patterns within species parallel those found across species (Bailey et al., 2009), we expect a dominant role for structuring by oak food plant.…”