Colonization of Marginal Host Plants by Seed Beetles (Coleoptera: Chrysomelidae): Effects of Geographic Source and Genetic Admixture

Abstract

The ability to adapt to a novel host plant may vary among insect populations with different genetic histories, and colonization of a marginal host may be facilitated by genetic admixture of disparate populations. We assembled populations of the seed beetle, Callosobruchus maculatus (F.), from four continents, and compared their ability to infest two hosts, lentil and pea. We also formed two cross-continent hybrids (Africa × N.A. and Africa × S.A.). In pre-selection assays, survival was only ~3% in lentil and ~40% in pea. For three replicate populations per line, colonization success on lentil was measured as cumulative exit holes after 75–175 d. On pea, we estimated the change in larval survival after five generations of selection. Females in all lines laid few eggs on lentil, and survival of F1 larvae was uniformly <5%. Subsequently, however, the lines diverged considerably in population growth. Performance on lentil was highest in the Africa × N.A. hybrid, which produced far more adults (mean > 11,000) than either parental line. At the other extreme, Asian populations on lentil appeared to have gone extinct. The Africa × N.A. line also exhibited the highest survival on pea, and again performed better than either parent line. However, no line displayed a rapid increase in survival on pea, as is sometimes observed on lentil. Our results demonstrate that geographic populations can vary substantially in their responses to the same novel resource. In addition, genetic admixtures (potentially caused by long-distance transport of infested seeds) may facilitate colonization of an initially poor host.

Evolution of developmental plasticity and the potential of host shift in the seed beetle: Insights from laboratory evolution experiments

“…In other words, evolution on the novel host for 35 years, resulted in a novel life‐history strategy for the seed beetle. Other examples of long‐term laboratory evolution on different hosts are also well known in Callosobruchus maculatus , where a response to selection was demonstrated for many different traits including lifetime fecundity, longevity, development time, and host acceptance (Fox et al, 2009; Gompert & Messina, 2016; Messina et al, 2009; Messina et al, 2020).…”

“…Presented results demonstrated significant divergence in both life-history traits and their plasticity between the P and C experimental groups. acceptance (Fox et al, 2009;Gompert & Messina, 2016;Messina et al, 2009;Messina et al, 2020). (Carrasco et al, 2015).…”

Disparate genetic variants associated with distinct components of cowpea resistance to the seed beetle Callosobruchus maculatus

“…Life-history and behavioral traits in the CA population are more typical for those of other geographic populations of C. maculatus. In contrast to SI females, CA females continue to add many eggs per seed (sometimes >10) when there are few available seeds (Messina et al, 2020). Moreover, larvae exhibit a tolerant or scramble-type competition within seeds (e.g., Mano and Toquenaga, 2008), so that a large, heavily infested seed can yield >10 adults, albeit of relatively small body size.…”

“…Inferences about genetic mechanisms underlying crop resistance to insects may depend on the particular assay used to measure pest performance, as well as the source of the pest population. This may be especially important for a cosmopolitan pest like C. maculatus, which consists of geographic populations ("biotypes") that are known to differ considerably in a suite of behavioral, physiological, and life-history traits, as well as in the range of crop species that they can infest (Messina, 1991;Messina et al, 2020). We therefore used two different assays that were intended to provide complementary estimates of cowpea resistance, as well two divergent pest populations.…”

“…A second assay estimated pest performance and F1 progeny production in a more realistic, competitive environment. For the second assay, we included C. maculatus populations known to differ in traits affecting host use and rates of infestation (Messina et al, 2018(Messina et al, , 2020.…”