Divergent host plant specialization as the critical driving force in speciation between populations of a phytophagous ladybird beetle

Detecting the isolating barrier that arises earliest in speciation is critically important to understanding the mechanism of species formation. We tested isolating barriers between host races of a phytophagous ladybird beetle, Henosepilachna diekei (Coleoptera: Coccinellidae: Epilachnine), that occur sympatrically on distinct host plants. We conducted field surveys for the distribution of the beetles and host plants, rearing experiments to measure six potential isolating factors (adult host preference, adult and larval host performance, sexual isolation, egg hatchability, F(1) hybrid inviability, and sexual selection against F(1) hybrids), and molecular analyses of mitochondrial ND2 and the nuclear ITS2 sequences. We found significant genetic divergence between the host races, and extremely divergent host preference (i.e. habitat isolation) and host performance (i.e. immigrant inviability), but no other isolating barriers. The fidelity to particular host plants arises first and alone can prevent gene flow between differentiating populations of phytophagous specialists.     

Herbivorous insects: model systems for the comparative study of speciation ecology

Does ecological divergence drive species-level evolutionary diversification? How so and to what degree? These questions were central to the thinking of the evolutionary synthesis. Only recently, however, has the ecology of speciation become an important focus of empirical study. Here, we argue that ecologically specialized, phylogenetically diverse, and experimentally tractable herbivorous insect taxa offer great opportunities to study the myriad mechanisms by which ecology may cause reproductive isolation and promote speciation. We call for the development and integrated experimental study of a taxonomic diversity of herbivore model systems and discuss the availability and recent evaluation of suitable taxa. Most importantly, we describe a general comparative framework that can be used to rigorously test a variety of hypotheses about the relative contributions and the macroevolutionary generality of particular mechanisms. Finally, we illustrate important issues for the experimental analysis of speciation ecology by demonstrating the consequences of specialized host associations for ecological divergence and premating isolation in Neochlamisus bebbianae leaf beetles.     

The Role of Adaptation to Host Plants in the Evolution of Reproductive Isolation: Negative Evidence from Tetranychus Urticae Koch

Reproductive isolation between demes of a phytophagous arthropod population that use different host plant species could evolve in two different ways. First, adaptation to different host species might result in reproductive isolation as a pleiotropic by-product. Second, if adaptation to one host species strongly reduces fitness on others, selection could favour mechanisms, such as host fidelity and assortative mating, that restrict gene flow between host-adapted demes. A laboratory selection experiment on the broadly polyphagous spider mite Tetranychus urticae gave information on these possibilities. A population allowed to adapt to tomato plants showed increased survival, development rate and fecundity on tomato relative to the base population from which it was derived. In spite of the large difference between the tomato-adapted and base populations in performance on tomato plants, the two populations showed no evidence of reproductive isolation, as measured by the hatching rate of eggs laid by F1 hybrids between the lines. Furthermore, a genetically variable population formed by hybridizing the tomato-adapted and base populations did not show evidence for a decline in ability to survive on tomato after more than ten generations of mass rearing on lima bean, indicating that tomato-adapted genotypes suffered little or no selective disadvantage on bean. These results give no support for the role of host plants in the evolution of reproductive isolation in T. urticae.     

The evolution of host preference in allopatric vs. parapatric populations of Timema cristinae walking-sticks

Divergent habitat preferences can contribute to speciation, as has been observed for host-plant preferences in phytophagous insects. Geographic variation in host preference can provide insight into the causes of preference evolution. For example, selection against maladaptive host-switching occurs only when multiple hosts are available in the local environment and can result in greater divergence in regions with multiple vs. a single host. Conversely, costs of finding a suitable host can select for preference even in populations using a single host. Some populations of Timema cristinae occur in regions with only one host-plant species present (in allopatry, surrounded by unsuitable hosts) whereas others occur in regions with two host-plant species adjacent to one another (in parapatry). Here, we use host choice and reciprocal-rearing experiments to document genetic divergence in host preference among 33 populations of T. cristinae. Populations feeding on Ceanothus exhibited a stronger preference for Ceanothus than did populations feeding on Adenostoma. Both allopatric and parapatric pairs of populations using the different hosts exhibited divergent host preferences, but the degree of divergence tended to be greater between allopatric pairs. Thus, gene flow between parapatric populations apparently constrains divergence. Host preferences led to levels of premating isolation between populations using alternate hosts that were comparable in magnitude to previously documented premating isolation caused by natural and sexual selection against migrants between hosts. Our findings demonstrate how gene flow and different forms of selection interact to determine the magnitude of reproductive isolation observed in nature.