Effects of crowding and host plant quality on morph determination in the soybean aphid,Aphis glycines

Abstract

Polyphenism constitutes a key example of the adaptability of a genotype to a shifting environment. In aphids, the relative production of apterous and alate individuals is influenced by cues resulting from increases in population density, changes in plant quality, and natural enemies. The ability to respond to multiple environmental cues offers aphids an effective way to optimize their fitness. Understanding the mechanisms behind alate morph production is particularly important in aphid species that are agricultural pests. We tested the effects of crowding and host plant quality cues on morph determination in Aphis glycines Matsumura (Hemiptera: Aphididae). We exposed A. glycines to pre-natal and post-natal crowding under laboratory conditions. In the field, we reared nymphs of A. glycines at high-density vs. low-density conditions in clip cages set on the top vs. bottom nodes of infested and uninfested soybean plants, Glycine max (L.) Merrill (Fabaceae). Apterous adult body size was used as an estimate of aphid performance, and the proportion of morphs developing under each condition was determined. Both pre-and post-natal crowding induced the production of asexual alate individuals by A. glycines. In the field, we observed additive negative effects of lower overall plant quality (infested vs. uninfested plants), within-plant differences in nutritional quality (bottom vs. top nodes), and high vs. low levels of crowding on aphid size. These three factors also interacted to increase the proportion A. glycines nymphs that developed wings. Our results suggest two levels in the production of asexual alate individuals by A. glycines: (1) a moderate level in response to aggregation, triggered by crowding cues, and (2) a high level in response to plant quality deterioration, triggered by both plant quality and crowding cues. These two processes ensure a flexible production of asexual alate individuals, allowing aphids to adapt to changing environmental conditions.

Comparative transcriptional analysis provides insights of possible molecular mechanisms of wing polyphenism induced by postnatal crowding in Aphis gossypii

“…This strategy is considered to have contributed to the evolutionary success of aphids. Alate morph, with long wings, flight muscles and flight capability, benefits for searching hosts, escaping from natural enemies and reducing negative density-dependent population effects through dispersal (Martínez and Costamagna 2018). Nonetheless, wingless morph, with absent wings and underdeveloped flight muscles, shows an earlier onset of oviposition and higher reproductive capacity, allowing a rapid increase of the aphid colony size (Castañeda et al 2010).…”

“…In wing-dimorphic aphid species, the production of asexual alate morphs resulted from increased population density, poor plant quality and natural enemies (Braendle et al 2006). Crowding is considered to be one major environmental factor in aphids wing induction, in which the production of wing is triggered by tactile stimuli between individual aphids (Forrest 1974;Kidd and Tozer 1984;Martínez and Costamagna 2018;Purandare et al 2014). Series of signal pathways were reported to participate in the wing differentiation induced by crowding in several aphid species, including ecdysone, juvenile hormone (JH), octopamine, olfactory receptors co-receptor (Ishikawa et al 2013;Jia et al 2015;Vellichirammal et al 2017;Wang et al 2016).…”

Transcriptome profiling of maternal stress‐induced wing dimorphism in pea aphids

“…Increasing physical contact of pea aphids in a certain range of density caused many winged progenies (Lees, 1967;Martinez & Costamagna, 2018). Previous studies have revealed that contact between conspecific aphids or stimulation with a paintbrush induces the production of winged offspring (Johnson, 1965;Purandare, Tenhumberg, & Brisson, 2014).…”

“…Maternal A. fabae aphids tended by the mutualistic ant Formica fusca produce a high proportion of wingless offspring, and this phenomenon might be related to a juvenile hormone-related chemical from the ants (Kleinjan & Mittler, 1975). Moreover, the high-density signaling increases the proportion of producing winged individuals in Aphis glycines, Megoura crassicauda, and A. pisum (Ishikawa, Gotoh, Abe, & Miura, 2013;Martinez & Costamagna, 2018;Wilkinson et al, 2016). Such maternal stress-induced wing dimorphism has been a research hotspot for more than a century.…”

Size matters in insects – an introduction

“…Hence, zucchini may be a better host for development of Z. cucurbitae. Rios Martinez & Costamagna (2018) investigate how crowding, host plant quality, and within-plant distribution affect morph determination in the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae). The authors experimentally altered density levels in the field and observed strong effects on adult body size which was used as an estimate of aphid performance.…”