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

J of Evolutionary Biology

Durham

2015

Experimental evolution has provided little support for the hypothesis that the narrow diets of herbivorous insects reflect trade-offs in performance across hosts; selection lines can sometimes adapt to an inferior novel host without a decline in performance on the ancestral host. An alternative approach for detecting trade-offs would be to measure adaptation decay after selection is relaxed, that is, when populations newly adapted to a novel host are reverted to the ancestral one. Lines of the seed beetle Callosobruchus maculatus rapidly adapted to a poor host (lentil); survival in lentil seeds increased from 2% to > 90% in < 30 generations. After the lines had reached a plateau with respect to survival in lentil, sublines were reverted to the ancestral host, mung bean. Twelve generations of reversion had little effect on performance in lentil, but after 25-35 generations, the reverted lines exhibited lower survival, slower development and smaller size. The most divergent pair of lines was then assayed on both lentil and mung bean. Performance on lentil was again much poorer in the reverted line than in the nonreverted one, but the lines performed equally well on mung bean. Moreover, the performance of the nonreverted line on mung bean remained comparable to that of the original mung-bean population. Our results thus present a paradox: loss of adaptation to lentil following reversion implies a trade-off, but the continued strong performance of lentil-adapted lines on mung bean does not. Genomic comparisons of the reverted, nonreverted and ancestral lines may resolve this paradox and determine the importance of selection vs. drift in causing a loss of adaptation following reversion.

Section: Methodsmentioning

confidence: 98%

Loss of adaptation following reversion suggests trade‐offs in host use by a seed beetle

J of Evolutionary Biology

Durham

2015

“…The Burkina Faso (BF) population is adapted to the larger cowpeas; larvae are scramble competitors and crowded seeds frequently yield multiple adults. Females are less deterred from egg laying by the presence of previously laid eggs, lay small eggs and exhibit fairly high size‐adjusted fecundity (Fox et al ., , ).…”

Section: Methodsmentioning

confidence: 99%

Evolution of larval competitiveness and associated life‐history traits in response to host shifts in a seed beetle

Fox

J of Evolutionary Biology

2018

Resource competition is frequently strong among parasites that feed within small discrete resource patches, such as seeds or fruits. The properties of a host can influence the behavioural, morphological and life-history traits of associated parasites, including traits that mediate competition within the host. For seed parasites, host size may be an especially important determinant of competitive ability. Using the seed beetle, Callosobruchus maculatus, we performed replicated, reciprocal host shifts to examine the role of seed size in determining larval competitiveness and associated traits. Populations ancestrally associated with either a small host (mung bean) or a large one (cowpea) were switched to each other's host for 36 generations. Compared to control lines (those remaining on the ancestral host), lines switched from the small host to the large host evolved greater tolerance of co-occurring larvae within seeds (indicated by an increase in the frequency of small seeds yielding two adults), smaller egg size and higher fecundity. Each change occurred in the direction predicted by the traits of populations already adapted to cowpea. However, we did not observe the expected decline in adult mass following the shift to the larger host. Moreover, lines switched from the large host (cowpea) to the small host (mung bean) did not evolve the predicted increase in larval competitiveness or egg size, but did exhibit the predicted increase in body mass. Our results thus provide mixed support for the hypothesis that host size determines the evolution of competition-related traits of seed beetles. Evolutionary responses to the two host shifts were consistent among replicate lines, but the evolution of larval competition was asymmetric, with larval competitiveness evolving as predicted in one direction of host shift, but not the reverse. Nevertheless, our results indicate that switching hosts is sufficient to produce repeatable and rapid changes in the competition strategy and fitness-related traits of insect populations.

“…At least some of the differences between the African and Asian populations appear to depend on the different properties of their respective hosts (Messina and Karren 2003, Messina 2004a, Fox et al 2009). The African population was collected in Burkina Faso from an infestation of cowpea, Vigna unguiculata (L.) Walpers (Messina 1993), and has been continuously reared on that host.…”

mentioning

confidence: 99%

Adaptation to a Novel Host by a Seed Beetle (Coleoptera: Chrysomelidae: Bruchinae): Effect of Source Population

Durham

2013

Environ Entomol

Self Cite

Geographic populations of a widespread species can differ in their ability to adapt to a novel environment because they possess different amounts of the requisite genetic variation. We compared responses to the same novel host in ecologically and genetically divergent populations of the seed beetle Callosobruchus maculatus (F.). Populations from Africa and Asia had been derived from and maintained on different legume hosts. In preselection assays, both populations exhibited lower survival, slower development, and smaller size on a third host (adzuki bean), and the difference in performance between the ancestral and novel hosts was especially high for the African population. Replicate lines of each population were switched to adzuki bean or maintained on the ancestral host, and beetle performance was measured on both hosts after 12 generations. Survival on adzuki bean increased substantially in the adzuki-bean lines of the African population, but improved only slightly in the Asian lines. Similarly, only the African adzuki-bean lines exhibited significantly faster development on adzuki bean. Improved performance on adzuki bean did not simultaneously reduce performance on the ancestral host. Together with previous studies, these results confirm that populations of C. maculatus often possess sufficient standing genetic variation for rapid adaptation to a novel host, but the magnitude of the response may depend on the source population. Although international trade in grain legumes can expand beetle host ranges and produce unusual biotypes, the consistent absence of strong genetic trade-offs in larval performance or adult oviposition across hosts makes it unlikely that this insect would form distinct host races.