Abstract
BackgroundThe evolution of reproductive isolation between herbivorous insect populations is often initiated by shifts to novel host-plants, a process that underlies some of the best examples of ecological speciation. However, it is not well understood why host-shifts occur. Arguably the most common hypothesis is that host-shifts occur in response to competition, while a less frequently invoked hypothesis is that herbivores adapt locally to geographic differences in potential host-plant communities. Here we investigate whether geographic variation in host-plant availability is likely to have driven host-shifts in restio leafhoppers. We studied local adaptation of a camouflaged restio leafhopper species, Cephalelus uncinatus, to host-plants in the Restionaceae (restios); a family of plants with exceptional diversity in the anomalously species-rich Cape Floristic Region (CFR). To determine whether C. uncinatus experiences heterogeneous host communities across its range, we first quantified the degree of geographic overlap between C. uncinatus and each of its associated host-plant species. Then we quantified trait divergence (host preference, body size and colour) for three pairs of C. uncinatus populations found on different host-plant species differing in their degree of spatial overlap. Spectral reflectance was modelled in bird visual space to investigate whether body colour divergence in C. uncinatus corresponds to leaf sheath colour differences between restio species as perceived by potential predators.ResultsWe demonstrate that C. uncinatus is forced to use different restio species in different regions because of turnover in available host species across its range. Comparisons between geographically separated populations were consistent with local adaptation: restio leafhoppers had preferences for local host-plants over alternative host-plants and matched local plants better in terms of size and colour.ConclusionsSpatial turnover in host-plant availability has likely facilitated host-shifts in C. uncinatus. Spatial turnover in host-plant availability may be an important driver of insect diversification in the CFR and globally.
Highlights
The evolution of reproductive isolation between herbivorous insect populations is often initiated by shifts to novel host-plants, a process that underlies some of the best examples of ecological speciation
Our study focuses on Cephalelus uncinatus, a broadly distributed restio leafhopper species which completes its entire life cycle on restios
Each host species was only present in 33% of the C. uncinatus range (48% upper 95% CI)
Summary
The evolution of reproductive isolation between herbivorous insect populations is often initiated by shifts to novel host-plants, a process that underlies some of the best examples of ecological speciation It is not well understood why host-shifts occur. Speciation by shifting hosts (when populations of parasites adapt to novel hosts [1,2,3]) is viewed as the primary mode of speciation in herbivorous insects (but see exceptions [4,5,6]) It is not well understood how host-shifts are initiated. Once the host-shift has occurred, geographic expansion into the distribution range of the newly colonised host species may ensue, sometimes creating largely allopatric distribution patterns We refer to this as the sympatric host-shift model (see Fig. 1a). This is the idea that has dominated the literature on host shifts by herbivorous insects [17, 18], despite the fact that herbivorous insects seldom reach densities where food is limiting [19]; perhaps making competition an infrequent driver of sympatric host shifts
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