Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera: Bruchidae): traits associated with stored‐product pest status

Abstract

Despite the fact that many plant-feeding insects are pests, little effort has been made to identify key evolutionary trait transitions that allow taxa to acquire or lose pest status. A large proportion of species in the genus Callosobruchus are economically important pests of stored, dry postharvest beans of the tribe Phaseoleae. However, the evolution of this feeding habit is poorly understood. Here, we present a reconstruction of the phylogeny of the Asian and African Callosobruchus based on three mitochondrial genes, and assess which traits have been associated with the evolutionary origin or loss of ability to reproduce on dry beans. Our phylogenetic analysis showed that species group into the chinensis and the maculatus clades, which are also supported by genital morphology, and an additional paraphyletic group. Ancestral ability to use dry beans has been lost in the chinensis clade but acquired again in C. chinensis. Dry-bean use and host-plant use were both phylogenetically constrained and transitions in the two were significantly correlated. Host shifts from the subtribe Phaseolinae to Cajaninae were more common than the reverse and were more likely in species using young beans. The ability to use dry beans was more likely gained when using Phaseolinae hosts and promoted habitat shifts from tropical to temperate regions. Adaptation to arid climate was also associated with the ability to reproduce on dry beans and on Phaseolinae. Thus, our analysis suggests that physiological adaptations to an arid climate and to Phaseolinae hosts both render beetles predisposed to become pests of cultivated beans.

Global legume diversity assessment: Concepts, key indicators, and strategies

“…Food webs of the legume-bruchine system have been studied in various geographic areas (Johnson, 1981a;Udayagiri & Wadhi, 1989;Kergoat & al., 2007a); Asia (Chujo, 1937;Arora, 1977;Tuda & al., 2005Tuda & al., , 2006, the Middle East (Johnson & al., 2004), Europe (Hoffmann, 1945;Jermy & Szentesi, 2003;Delobel & Delobel, 2006;Kergoat & al., 2007b), Africa (Johnson & al., 2004;Kergoat & al., 2005), Russia (Luk'yanovich & Ter-Minasyan, 1957) and the New World (North and Central America, Johnson, 1970Johnson, , 1983Kingsolver, 2004;Kato & al., 2010;South America, Johnson, 1990). Native bruchines are absent in arctic areas and Pacific islands and scarce in Australia (Borowiec, 1987).…”

Genetic architecture underlying convergent evolution of egg-laying behavior in a seed-feeding beetle

“…Both populations had been maintained in the laboratory on their ancestral hosts for [100 generations prior to the original selection experiment, and were thus likely to have reached genetic equilibrium with respect to the laboratory environment (Harshman and Hoffmann 2000). Laboratory conditions provide a reasonably close approximation of the 'natural' environment of C. maculatus, which has infested human stores of grain legumes for thousands of years and displays specific traits for exploiting grain-legume seeds both in the field and in storage (Tuda et al 2006).…”

Applied evolutionary ecology of insects of the subfamily Bruchinae (Coleoptera: Chrysomelidae)

“…Long dry season was shown to be the most important factor for evolution towards preadaptive stage to become stored bean pests (i.e., ability to use dry hard beans) when evolutionary history was accounted for (Tuda et al, 2006). Phylogenetic history of Callosobruchus and idiosyncrasy of their host plants also had significant effects on the evolution towards stored bean pests (Tuda et al, 2006). In future studies, hardness of dried seeds will be one of the foci of research because the hardness per se can serve as a deterrent against seed predators, including bean beetles (Janzen, 1977;Southgate, 1979;Kitch et al, 1991;Dongre et al, 1993).…”

“…External and internal morphology of the adult stage is used for identification to species. Most recently male genital traits for Callosobruchus were compared and summarized by Tuda et al (2006). Compared to adult morphology, egg and larval morphology is less well studied because they are not readily available (but see Pfaffenberger and Johnson, 1976;Arora, 1978;Delobel et al, 1995b), which makes identification based on pre-adult stages difficult.…”

“…Using a comparative approach to study Callosobruchus pest and nonpest species, the potential effects of climate, host plants, phylogeny and endosymbiotic bacterium were examined (Tuda et al, 2006). Long dry season was shown to be the most important factor for evolution towards preadaptive stage to become stored bean pests (i.e., ability to use dry hard beans) when evolutionary history was accounted for (Tuda et al, 2006). Phylogenetic history of Callosobruchus and idiosyncrasy of their host plants also had significant effects on the evolution towards stored bean pests (Tuda et al, 2006).…”