- Evolutionary Dynamics, Instituto Gulbenkian de Ciência (IGC), Oeiras, Portugal
- Climate change, Evolutionary ecology, Life history, Molecular ecology, Morphometrics, Phenotypic plasticity, Population ecology
Host-mediated, cross-generational intraspecific competition in a herbivore species
Plants preserve the ghost of competition past for herbivores, but mothers don’t care
Some biological hypotheses are widely popular, so much so that we tend to forget their original lack of success. This is particularly true for hypotheses with catchy names. The ‘Ghost of competition past’ is part of the title of a paper by the great ecologist, JH Connell, one of the many losses of 2020 (Connell 1980). The hypothesis states that, even though we may not detect competition in current populations, their traits and distributions may be shaped by past competition events. Although this hypothesis has known a great success in the ecological literature, the original paper actually ends with “I will no longer be persuaded by such invoking of "the Ghost of Competition Past"”. Similarly, the hypothesis that mothers of herbivores choose host plants where their offspring will have a higher fitness was proposed by John Jaenike in 1978 (Jaenike 1978), and later coined the ‘mother knows best’ hypothesis. The hypothesis was readily questioned or dismissed: “Mother doesn't know best” (Courtney and Kibota 1990), or “Does mother know best?” (Valladares and Lawton 1991), but remains widely popular. It thus seems that catchy names (and the intuitive ideas behind them) have a heuristic value that is independent from the original persuasion in these ideas and the accumulation of evidence that followed it.
The paper by Castagneryol et al. (2021) analyses the preference-performance relationship in the box tree moth (BTM) Cydalima perspectalis, after defoliation of their host plant, the box tree, by conspecifics. It thus has bearings on the two previously mentioned hypotheses. Specifically, they created an artificial population of potted box trees in a greenhouse, in which 60 trees were infested with BTM third instar larvae, whereas 61 were left uninfested. One week later, these larvae were removed and another three weeks later, they released adult BTM females and recorded their host choice by counting egg clutches laid by these females on the plants. Finally, they evaluated the effect of previously infested vs uninfested plants on BTM performance by measuring the weight of third instar larvae that had emerged from those eggs.
This experimental design was adopted because BTM is a multivoltine species. When the second generation of BTM arrives, plants have been defoliated by the first generation and did not fully recover. Indeed, Castagneryol et al. (2021) found that larvae that developed on previously infested plants were much smaller than those developing on uninfested plants, and the same was true for the chrysalis that emerged from those larvae. This provides unequivocal evidence for the existence of a ghost of competition past in this system. However, the existence of this ghost still does not result in a change in the distribution of BTM, precisely because mothers do not know best: they lay as many eggs on plants previously infested than on uninfested plants.
The demonstration that the previous presence of a competitor affects the performance of this herbivore species confirms that ghosts exist. However, whether this entails that previous (interspecific) competition shapes species distributions, as originally meant, remains an open question. Species phenology may play an important role in exposing organisms to the ghost, as this time-lagged competition may have been often overlooked. It is also relevant to try to understand why mothers don’t care in this, and other systems. One possibility is that they will have few opportunities to effectively choose in the real world, due to limited dispersal or to all plants being previously infested.
Castagneyrol, B., Halder, I. van, Kadiri, Y., Schillé, L. and Jactel, H. (2021) Host-mediated, cross-generational intraspecific competition in a herbivore species. bioRxiv, 2020.07.30.228544, ver. 5 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.07.30.228544
Connell, J. H. (1980). Diversity and the coevolution of competitors, or the ghost of competition past. Oikos, 131-138. doi: https://doi.org/10.2307/3544421
Courtney, S. P. and Kibota, T. T. (1990) in Insect-plant interactions (ed. Bernays, E.A.) 285-330.
Jaenike, J. (1978). On optimal oviposition behavior in phytophagous insects. Theoretical population biology, 14(3), 350-356. doi: https://doi.org/10.1016/0040-5809(78)90012-6
Valladares, G., and Lawton, J. H. (1991). Host-plant selection in the holly leaf-miner: does mother know best?. The Journal of Animal Ecology, 227-240. doi: https://doi.org/10.2307/5456