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Corresponding author: Vincent A. D. Hervet ( vincent.hervet@gmail.com ) Academic editor: Jose Fernandez-Triana
© 2018 Vincent A. D. Hervet, Robert A. Laird, Kevin D. Floate.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Hervet VAD, Laird RA, Floate KD (2018) Siblicidal behaviour by larvae of the gregarious parasitoid Cotesia vanessae. Journal of Hymenoptera Research 67: 55-62. https://doi.org/10.3897/jhr.67.28978
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Contrasting life histories distinguish solitary from gregarious parasitoids. Females of solitary species typically lay one egg in a host; when more than one parasitoid is present in the host, larvae will kill their rivals so that only one parasitoid completes development. Females of gregarious species typically lay multiple eggs in the same host with the resultant larvae co-existing to complete development. Here we provide an unusual report of siblicide by larvae of a gregarious parasitoid; i.e., Cotesia vanessae (Reinhard) (Hymenoptera: Braconidae) developing in noctuid caterpillars (Lepidoptera). Siblicidal behaviour has not previously been reported with larvae of gregarious Braconidae. We speculate that this behaviour reflects a trade-off between the finite amount of resources within the host available for larval development, and selection to optimize use of these resources. ‘Flooding’ the host with eggs allows the female to use the finite resources of the host to their fullest extent, regardless of host size. This strategy also may allow the female to overwhelm the host’s immune system to enhance survival of her progeny in otherwise marginal host species. It further may enhance the ability of the female’s progeny to competitively exclude the larvae of conspecific females or larvae of other parasitoid species co-occurring in the host. Siblicide allows for self-regulation of brood size when host resources are insufficient to support egg-to-adult development of all eggs initially laid in the host.
Trichoplusia ni , competitive exclusion, siblicide, host-parasitoid interaction, Braconidae , Noctuidae
A finite amount of resources are available within a host to support parasitoid development. Gregarious parasitoids typically lay multiple eggs per host, whereas solitary parasitoids typically lay one egg per host. Resource competition arises when a parasitoid lays multiple eggs in the host during one ovipositional bout, when conspecific gregarious or solitary parasitoids parasitize the same individual host multiple times (superparasitism), or when multiple species oviposit in the same individual host (multiparasitism).
Competition can take various forms along a continuum defined by extremes of scramble competition versus contest competition (
Here we report high rates of siblicide among larvae of the gregarious parasitoid Cotesia vanessae (Reinhard) (Hymenoptera: Braconidae). Comprised of both sexual and parthenogenetic populations (
In previous experiments using a parthenogenetic population, we assessed a range of lepidopteran species as potential hosts for C. vanessae by parasitizing early 4th instar caterpillars. Female C. vanessae were placed in contact with the caterpillar until a single bout of oviposition was observed. The parasitized caterpillars were then reared on an artificial diet (
To better understand the factors that affect parasitoid emergence, we dissected parasitized caterpillars of three species. Dissections were performed up to 11 days after exposure to parasitism. For these dissections, the head and the last rear abdominal segments of each caterpillar were excised and the digestive system removed. Haemolymph was then squeezed from the hemocoel onto a microscope slide, diluted with one drop of saline solution, topped with a coverslip, and examined using a compound light microscope (400×). Some caterpillars dissected immediately after parasitism had large fat bodies that clouded the haemolymph and hindered observations. Thereafter, caterpillars were held for 2 days without food prior to dissections. This method allowed for easy viewing of egg and larvae stages (Fig.
The species selected for dissections were cabbage looper (Trichoplusia ni (Hübner)) (n = 20), true armyworm (Mythimna unipuncta (Haworth)) (> 10), and the corn earworm (Helicoverpa zea (Boddie)) (Lepidoptera: Noctuidae) (n = 17). Our previous experiments identified these species to be ‘good’, ‘medium’ and ‘poor’ hosts, respectively (
Our observations on the dissected caterpillars showed both teratocyte production and encapsulation to affect the survival of immature C. vanessae (Fig.
Unexpectedly, caterpillars of all three lepidopteran species contained many dead first instar parasitoids that were bisected in the transverse plane (Fig.
Gregariousness has evolved multiple times from solitary ancestors within the genus Cotesia and in other parasitoid taxa, typically accompanied by a loss of antagonistic behaviour toward siblings and a loss of motility (
Motility of first instar solitary species is typically enabled by a caudal appendage (
Immature stages of Cotesia vanessae in caterpillars of three lepidopteran species. A Egg (parts of adjacent eggs visible on left and top sides), with visible extraembryonic membrane made of large cells that will become teratocytes (within Trichoplusia ni, five days post-oviposition) B Neonate larva with teratocytes (t) (within T. ni, five days post-oviposition). Head on the left, anal vesicle (av) on the right, thoracic and first 7 abdominal segments each partly surrounded on their dorsal and lateral sides by a row of cuticular spines projecting backward C Egg becoming encapsulated by hemocytes (within Helicoverpa zea, four days post-oviposition) D Encapsulated first-instar larva (within H. zea, eleven days post-oviposition) E Front of head (within T. ni, eight days post-oviposition). Microscope focused on mandibles (m) F First-instar larva (on its side), with four pieces of bisected larvae (bl) nearby (within Mythimna unipuncta, seven days post-parasitism) G Larva biting a sibling, with fore-half of bisected larva nearby (centre right) (within M. unipuncta, seven days post-oviposition). (Photo credit: Photo B by S. Harris, Agriculture and Agri-Food Canada, Saskatoon, SK; all other photos by V.A.D. Hervet.)
The laying of supernumerary eggs combined with reduced mobility of antagonistic first instars means that for C. vanessae it is not the mother wasp but its offspring that adjust brood size according to the available resources. The existence of this parent-offspring conflict could mean that C. vanessae larvae still have to evolve kin tolerance, which would enable female wasps to lay fewer eggs into hosts, all of which could survive to maturity, but it may also be that this strategy confers an advantage to this species. Laying hundreds of eggs in the same individual in one oviposition bout will generally optimize the use of available resources, regardless of host size. On one hand, large clutches enable the development of large broods in those hosts that allow for it. On the other hand, siblicide reduces scramble competition and acts as a safety mechanism to prevent the death of the whole brood in hosts that do not have sufficient resources for the development of all eggs laid (
It is interesting to speculate on the factors that could trigger larval siblicide. Presumably these include physical or chemical cues associated with the immature parasitoids. Arguably, the likelihood of physical contact or the concentration of chemical cues would be greater in a ‘good’ host (e.g., T. ni) than in a ‘poor’ host (e.g., H. zea); the immune system of the latter killing many first instars. We also note that our observations are based on a parthenogenetic population of C. vanessae for which all immatures within the host are essentially clones. Comparison of siblicide behaviour between parthenogenetic versus bisexual populations might prove enlightening. For example, what are the implications for larval siblicide on adult sex ratios in host species of different quality?
Cotesia vanessae has a broad range of lepidopteran hosts within the Noctuidae and Nymphalidae, including many species that are important economic pests of crops (
We thank Paul Coghlin, Bob Byers, John Dedes, Kayla Johnson, Jayden Dyck, Briana Smith, Marko Mićović, Abbey Brusky, and Braidon Schaufert for technical assistance, as well as Henry Murillo for sending us parasitoids and Stephanie Harris for allowing us to publish one of her pictures. This research was supported by the Canola Council of Canada (Canola Agronomic Research Program Project 2012–1, to K.D.F.), Alberta Conservation Association (Grants in Biodiversity, to V.A.D.H.), and the Natural Science and Engineering Research Council of Canada (Discovery Grant, to R.A.L.). This is Lethbridge Research and Development Centre Publication No. 38718052.