Shaking Youngsters and Shaken Adults: Female Beetles Eavesdrop on Larval Seed Vibrations to Make Egg-Laying Decisions

Abstract

Egg-laying decisions are critical for insects, and particularly those competing for limited resources. Sensory information used by females to mediate egg-laying decisions has been reported to be primarily chemical, but the role of vibration has received little attention. We tested the hypothesis that vibrational cues produced by feeding larvae occupying a seed influences egg-laying decisions amongst female cowpea beetles. This hypothesis is supported by three lines of evidence using two strains of the cowpea beetle (Callosobruchus maculatus), an Indian strain with choosy females and aggressively competing larvae and a Brazilian strain with less choosy females and larvae exhibiting an “accommodating” type of competition. First, in free-choice bioassays of seed selection, choosy Indian females selected control seeds (free of eggs, larvae, or egg-laying marker) over seeds with live larvae (free of eggs and egg-laying marker), but did not discriminate between control seeds and those with dead larvae. In contrast, less choosy Brazilian females showed no preference for seeds containing live or dead larvae over controls. Second, laser-doppler vibrometer recordings confirmed that larvae feeding inside seeds generate vibrations that are available to the female during egg-laying decisions. Third, during dichotomous choice experiments where artificial vibrations approximating those produced by feeding larvae were played back during seed selection, Indian females preferred immobile control seeds over vibrating seeds, but Brazilian females showed no preference. These results support the hypothesis that females use larval vibrations in their egg-laying decisions; whether these vibrations are passive cues exploited by the female, or active signals that ‘steer’ the behaviour of the female is unknown. We propose that vibration cues and signals could be important for host selection in insects, particularly those laying on substrates where visual or chemical cues may be unreliable. This seems to be the case with females of the cowpea beetle since visual cues are not important and chemical egg-marking does not last more than two weeks, allowing vibration cues to improve discrimination of egg-laying substrate particularly by choosy females.

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

“…These larvae tend to avoid interacting with each other within seeds, and actively construct “walls” to decrease the chance that their burrows will intersect (Mano & Toquenaga, ,b). In these populations, females will readily lay additional eggs on occupied seeds (Messina & Mitchell, ; Horng, ; Guedes & Yack, ). In other populations, larvae exhibit aggressive contest interactions within seeds; larvae fight within seeds, so that small‐ and even medium‐sized seeds often yield only one adult (Messina, ; Toquenaga et al ., ).…”

Evolution of host plant use and diversification in a species complex of parasitic weevils (Coleoptera: Curculionidae)

“…Mediated by marking pheromones, many parasitoids and phytophagous insects avoid hosts already infested by conspecifics or closely related species (Anderson, 2003; Nufio & Papaj, 2001; Roitberg & Prokopy, 1987). In beetles, there is evidence that ovipositing females of some species within the families Chrysomelidae (Guedes & Yack, 2016; Messina & Renwick, 1985) and Curculionidae (Addesso et al, 2007; Ferguson et al, 1999) avoid hosts and plant structures that have been previously utilized by other females for laying eggs. Hence, driven by chemical constraints, the use of a restricted set of host plants over evolutionary time scales may lead to inter- and intraspecific competition which in turn could facilitate an escape-and-radiate scenario (Ehrlich & Raven, 1964) where weevils “escape” to different plant structures, potentially undergoing diversification.…”

Mechanism of Resistance in Mungbean [Vigna radiata (L.) R. Wilczek var. radiata] to bruchids, Callosobruchus spp. (Coleoptera: Bruchidae)

“…The bruchids use vibrations from the egg laying substrates for oviposition ( Messina and Renwick, 1985 ; Messina, 2004 ; Guedes and Yack, 2016 ). Bruchids do not feed during the brief adult stage and reproduction depends mainly on the resources the insect accesses during larval stages from a single seed, with severe competition from other larvae ( Messina, 2004 ; Guedes et al, 2007 ).…”

“…Bruchids do not feed during the brief adult stage and reproduction depends mainly on the resources the insect accesses during larval stages from a single seed, with severe competition from other larvae ( Messina, 2004 ; Guedes et al, 2007 ). To avoid fierce larval competition in future—which may occur even inside the seeds, allowing only the emergence of larvae with good fitness—females lay a large number of eggs, depending on the substrate quality that the female perceives ( Messina, 2004 ; Guedes et al, 2007 ; Guedes and Yack, 2016 ). A good quality substrate will lead to good larval fitness and a successful population build-up.…”

“…A good quality substrate will lead to good larval fitness and a successful population build-up. Female bruchids have the ability to check the host suitability, deposit proper egg load, and discriminate the eggs laid by other females on a seed ( Oshima et al, 1973 ; Messina, 2004 ; Guedes and Yack, 2016 ). The females use various tactile, chemical, and physical cues to choose suitable egg-laying substrate.…”