Coevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habits
Abstract Background Animals use diverse antipredator mechanisms, including visual signalling of aversive chemical defence (aposematism). However, the initial evolution of aposematism poses the problem that the first aposematic individuals are conspicuous to predators who have not learned the signifi...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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BMC
2021-02-01
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| Series: | BMC Ecology and Evolution |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12862-020-01738-w |
| _version_ | 1818358220641533952 |
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| author | Lingzi Wang Stephen J. Cornell Michael P. Speed Kevin Arbuckle |
| author_facet | Lingzi Wang Stephen J. Cornell Michael P. Speed Kevin Arbuckle |
| author_sort | Lingzi Wang |
| collection | DOAJ |
| description | Abstract Background Animals use diverse antipredator mechanisms, including visual signalling of aversive chemical defence (aposematism). However, the initial evolution of aposematism poses the problem that the first aposematic individuals are conspicuous to predators who have not learned the significance of the warning colouration. In one scenario, aposematism evolves in group-living species and originally persisted due to kin selection or positive frequency-dependent selection in groups. Alternatively, group-living might evolve after aposematism because grouping can amplify the warning signal. However, our current understanding of the evolutionary dynamics of these traits is limited, leaving the relative merit of these scenarios unresolved. Results We used a phylogenetic comparative approach to estimate phenotypic evolutionary models to enable inferences regarding ancestral states and trait dynamics of grouping and aposematic colouration in a classic model system (caterpillars). We find strong support for aposematism at the root of the clade, and some (but weaker) support for ancestral solitary habits. Transition rates between aposematism and crypsis are generally higher than those between group-living and solitary-living, suggesting that colouration is more evolutionarily labile than aggregation. We also find that the transition from group-living to solitary-living states can only happen in aposematic lineage, suggesting that aposematism facilitates the evolution of solitary caterpillars, perhaps due to the additional protection offered when the benefits of grouping are lost. We also find that the high frequency of solitary, cryptic caterpillars is because this state is particularly stable, in that the transition rates moving towards this state are substantially higher than those moving away from it, favouring its accumulation in the clade over evolutionary time. Conclusions Our results provide new insights into the coevolution of colour and aggregation in caterpillars. We find support for an aposematic caterpillar at the root of this major clade, and for the signal augmentation hypothesis as an explanation of the evolution of aposematic, group-living caterpillars. We find that colouration is more labile than aggregation behaviour, but that the combination of solitary and cryptic habits is particularly stable. Finally, our results reveal that the transitions from group-living to solitary-living could be facilitated by aposematism, providing a new link between these well-studied traits. |
| first_indexed | 2024-12-13T20:25:33Z |
| format | Article |
| id | doaj.art-aabc88c8d0dd4929b8c34427bb01c8f5 |
| institution | Directory Open Access Journal |
| issn | 2730-7182 |
| language | English |
| last_indexed | 2024-12-13T20:25:33Z |
| publishDate | 2021-02-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Ecology and Evolution |
| spelling | doaj.art-aabc88c8d0dd4929b8c34427bb01c8f52022-12-21T23:32:34ZengBMCBMC Ecology and Evolution2730-71822021-02-012111910.1186/s12862-020-01738-wCoevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habitsLingzi Wang0Stephen J. Cornell1Michael P. Speed2Kevin Arbuckle3Institute of Integrative Biology, University of LiverpoolInstitute of Integrative Biology, University of LiverpoolSchool of Life Science, University of LiverpoolDepartment of Biosciences, College of Science, Swansea UniversityAbstract Background Animals use diverse antipredator mechanisms, including visual signalling of aversive chemical defence (aposematism). However, the initial evolution of aposematism poses the problem that the first aposematic individuals are conspicuous to predators who have not learned the significance of the warning colouration. In one scenario, aposematism evolves in group-living species and originally persisted due to kin selection or positive frequency-dependent selection in groups. Alternatively, group-living might evolve after aposematism because grouping can amplify the warning signal. However, our current understanding of the evolutionary dynamics of these traits is limited, leaving the relative merit of these scenarios unresolved. Results We used a phylogenetic comparative approach to estimate phenotypic evolutionary models to enable inferences regarding ancestral states and trait dynamics of grouping and aposematic colouration in a classic model system (caterpillars). We find strong support for aposematism at the root of the clade, and some (but weaker) support for ancestral solitary habits. Transition rates between aposematism and crypsis are generally higher than those between group-living and solitary-living, suggesting that colouration is more evolutionarily labile than aggregation. We also find that the transition from group-living to solitary-living states can only happen in aposematic lineage, suggesting that aposematism facilitates the evolution of solitary caterpillars, perhaps due to the additional protection offered when the benefits of grouping are lost. We also find that the high frequency of solitary, cryptic caterpillars is because this state is particularly stable, in that the transition rates moving towards this state are substantially higher than those moving away from it, favouring its accumulation in the clade over evolutionary time. Conclusions Our results provide new insights into the coevolution of colour and aggregation in caterpillars. We find support for an aposematic caterpillar at the root of this major clade, and for the signal augmentation hypothesis as an explanation of the evolution of aposematic, group-living caterpillars. We find that colouration is more labile than aggregation behaviour, but that the combination of solitary and cryptic habits is particularly stable. Finally, our results reveal that the transitions from group-living to solitary-living could be facilitated by aposematism, providing a new link between these well-studied traits.https://doi.org/10.1186/s12862-020-01738-wAposematicCoevolutionCrypticGroupPhenotypic evolutionSolitary |
| spellingShingle | Lingzi Wang Stephen J. Cornell Michael P. Speed Kevin Arbuckle Coevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habits BMC Ecology and Evolution Aposematic Coevolution Cryptic Group Phenotypic evolution Solitary |
| title | Coevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habits |
| title_full | Coevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habits |
| title_fullStr | Coevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habits |
| title_full_unstemmed | Coevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habits |
| title_short | Coevolution of group-living and aposematism in caterpillars: warning colouration may facilitate the evolution from group-living to solitary habits |
| title_sort | coevolution of group living and aposematism in caterpillars warning colouration may facilitate the evolution from group living to solitary habits |
| topic | Aposematic Coevolution Cryptic Group Phenotypic evolution Solitary |
| url | https://doi.org/10.1186/s12862-020-01738-w |
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