Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding

Abstract

Plant defenses against herbivores are predicted to change as plant lineages diversify, and with domestication and subsequent selection and breeding in the case of crop plants. We addressed whether defense against a specialist herbivore declined coincidently with life history evolution, domestication, and breeding within the grass genus Zea (Poaceae). For this, we assessed performance of corn leafhopper (Dalbulus maidis) following colonization of one of four Zea species containing three successive transitions: the evolutionary transition from perennial to annual life cycle, the agricultural transition from wild annual grass to primitive crop cultivar, and the agronomic transition from primitive to modern crop cultivar. Performance of corn leafhopper was measured through seven variables relevant to development speed, survivorship, fecundity, and body size. The plants included in our study were perennial teosinte (Zea diploperennis), Balsas teosinte (Zea mays parviglumis), a landrace maize (Zea mays mays), and a hybrid maize. Perennial teosinte is a perennial, iteroparous species, and is basal in Zea; Balsas teosinte is an annual species, and the progenitor of maize; the landrace maize is a primitive, genetically diverse cultivar, and is ancestral to the hybrid maize; and, the hybrid maize is a highly inbred, modern cultivar. Performance of corn leafhopper was poorest on perennial teosinte, intermediate on Balsas teosinte and landrace maize, and best on hybrid maize, consistent with our expectation of declining defense from perennial teosinte to hybrid maize. Overall, our results indicated that corn leafhopper performance increased most with the agronomic transition, followed by the life history transition, and least with the domestication transition.

Physical leaf defenses – altered by Zea life‐history evolution, domestication, and breeding – mediate oviposition preference of a specialist leafhopper

“…Our study indicated that the specialist herbivore D. maidis has a clear preference for maize over the teosintes, which suggests a lower level of anti-herbivore defense in the former, as suggested previously, also for other insects (Rosenthal & Dirzo, 1997;Szczepaniec et al, 2012;Takahashi et al, 2012;D avila-Flores et al, 2013). Additionally, our study did not address differences in chemical defenses nor nutritional value among host plants, which may further explain the oviposition preference that we found.…”

“…At the highest trichome density found in this study, one trichome per 1.9 mm (ca. Although our study does not shed light on the relevance of these hypotheses to our results, a recent study involving D. maidis and the suite of Zea plants studied herein suggests that host preference may be mediated by offspring performance because the performance of D. maidis was better on maizes compared to teosintes (D avila-Flores et al, 2013). 3 mm long 9 1 mm wide may still have sufficient space to maneuver unimpeded over the leaf surface, between trichomes, to feed and lay eggs.…”

“…Together, these results indicate that D. maidis is able to penetrate the toughest tissue, i.e., midrib, of any of the host plants with their mouthparts (stylets), suggesting that leaf blade toughness may be an unlikely defense against feeding by D. maidis. A study by D avila-Flores et al (2013) indeed showed that juvenile performance suffered on teosintes compared to maizes, but did not identify causes of the poorer performance of D. maidis, whether chemical or physical defenses, or nutritional differences among host plants. The inability to successfully develop on plants other than Zea in those studies may have been due to a combination of factors, such as physical incapability of the nymphs to feed from hosts with tougher leaves and thicker epidermises (Walker, 1985), or an inability to overcome the plant's chemical defenses.…”

Crop domestication, global human-mediated migration, and the unresolved role of geography in pest control

“…Insect herbivores typically perform better on agricultural plants than on wild ancestors, due to reductions in secondary compounds during crop domestication (Harvey et al, 2007;Rodriguez-Saona et al, 2011;Dávila-Flores et al, 2013;Szczepaniec et al, 2013;Turcotte et al, 2014). Crop domestication may facilitate herbivore populations in other ways as well.…”

Trophic interactions on <em>Zea</em> spp. plants involving the herbivores <em>Spodoptera frugiperda</em> (J.E. Smith), <em>Diatraea saccharalis</em> (Fabricius) and the predator <em>Doru luteipes</em> Scudder

“…Selective breeding reduces genetic diversity of domesticated crops, which results in lacking or weakly defensive traits (DOEBLEY et al, 2004 DIRZO, 1997;TAMIRU et al, 2011;SZCZEPANIEC et al, 2013;DÁVILA-FLORES et al, 2013;MUTYAMBAI et al, 2015). Hence, plant domestication also affects species interactions in tritrophic systems (BENREY et al, 1998;CHEN et al, 2015).…”