Data from: The Red Queen unveils the sexual and mating strategies of flowers
Authors/Creators
- 1. Universidade Federal do Rio Grande do Norte
- 2. Philipps University of Marburg
- 3. Swiss Federal Institute for Forest, Snow and Landscape Research
Description
The Red Queen Hypothesis states that sex evolved as an adaptation of hosts against their parasites, allowing them to produce offspring protected by rare combinations of defence-genes. It has been hypothesized that plant species under higher pressure by short-lived natural enemies should invest more heavily in outcrossing. Here, we test the interspecific prediction that plant species associated with a higher richness of insect herbivores – used as a proxy for a higher, more diverse and consistent herbivory pressure over geographic space and evolutionary time – should exhibit sexual and mating traits leading to outcrossing. We predict that plant species associated with a richer insect fauna will have a higher probability to be auto-incompatible, dichogamous, heterostylous, dimorphic, dioecious, and allogamous. Furthermore, they are predicted to exhibit a higher pollen-ovule ratio, to be more dependent on pollinators or wind for cross-fertilization, and to rely mostly on sexually-generated seeds for reproduction rather than on asexual means of reproduction.
In order to perform such comparative tests, we assembled published insect-plant interaction records and information on key reproductive floral traits linked to the inbreeding-outcrossing gradient for 1884 native angiosperm species from Germany. The analyses were performed with generalized linear models and phylogenetic models using species richness of insect herbivores as the single explanatory variable, but also with plant geographic range size and plant height as covariates.
We showed that plant species consumed by a higher species richness of insect herbivores have a higher probability to be auto-incompatible, dichogamous, dimorphic, dioecious, and allogamous. In addition, they had a higher pollen-ovule ratio, were more dependent on pollinators or wind for cross-fertilization, and relied mostly on sexually-generated seeds for reproduction rather than also use asexual reproduction. Model fitting improved considerably after taking into consideration the phylogenetic structure of the data and the results remained relatively consistent after controlling for geographic range size and plant height.
Synthesis. Although the conventional wisdom is that floral traits of plants evolved in concert with their mutualistic pollinators, here we showed that several key sexual and mating traits of plants, which modulate their outcrossing strategy, evolved in response to the pressure exerted by their antagonistic insect herbivores. The Red Queen Hypothesis emerges as a unifying theory which helps to explain the sexual diversity of angiosperms, with consequences for genetic and phylogenetic diversity, animal-plant network structures, and plant-based ecosystem services.
Notes
Funding provided by: Coordenação de Aperfeicoamento de Pessoal de Nível Superior
ROR ID: https://ror.org/00x0ma614
Award Number: 88887.897122/2023-00
Funding provided by: National Council for Scientific and Technological Development
ROR ID: https://ror.org/03swz6y49
Award Number: PQ-308657/2023-3
Funding provided by: Deutsche Forschungsgemeinschaft
ROR ID: https://ror.org/018mejw64
Award Number: 310030E-173542/1
Funding provided by: Swiss National Science Foundation
ROR ID: https://ror.org/00yjd3n13
Award Number: 310030E-173542
Methods
METHODS
Our dataset focused on flowering plants from Germany, where insect-plant interaction associations have been recorded for centuries with the contribution of naturalists, botanists and entomologists and this knowledge has been organized as large publications and online datasets. To test the Red Queen predictions, we compiled species-level data on ten key reproductive traits that can modulate the inbreeding/outcrossing level of plants as well as information on plant-insect herbivore interactions to estimate the richness of insect herbivores associated with each plant species.
Ten response variables were considered: (a) Self-incompatibility (binary; [0] self-compatible, [1] self-incompatible), (b) Dichogamy (binary; [0] synchronous, [1] asynchronous), (c) Heterostily (binary; [0] homostylous, [1] heterostylous), (d) Sexual dimorphism (binary; [0] monomorphic, [1] dimorphic), (e) Sexual system (ordinal; [0] hermaphrodite, [1] andromonoecy and gynomonoecy, [2] diclinous monoecy, [3] androdioecy, gynodioecy and trioecy, [4] dioecy), (f) Breeding system (ordinal; [0] autogamy, [1] facultative autogamy, [2] mixed mating, [3] facultative allogamy, [4] allogamy), (g) Pollen-ovule ratio (continuous; pollen number / ovule number; log10-scale), (h) Insect dependence (ordinal; [0] rarely [1] often and [2] always insect-pollinated), (i) Wind dependence (ordinal; [0] rarely, [1] often and [2] always wind-pollinated), (j) Reproductive strategy (binary; [0] vegetative and seed reproduction, [1] reproduction by seed). Notice that all variables were ordered from a higher probability of selfing to a higher probability of outcrossing. The plant traits were mainly extracted from the databases BiolFlor, a comprehensive database on biological and ecological traits of the German flora (Kühn et al., 2004. http://doi.org/10.1111/j.1366-9516.2004.00106.x), LEDA, a database of life-history traits of the Northwest European flora (Kleyer et al., 2008. https://doi.org/10.1111/j.1365-2745.2008.01430.x), and TRY, a global database of curated plant traits (https://www.try- db.org/TryWeb/Home.php). For pollen-ovule ratio, we complemented the data by performing literature search. In some analyses, we used geographic range size and plant height as covariates. Geographic range size was estimated by the area of occupancy of the plants obtained from the FloraWeb, expressed as numbers of TK25 quadrats occupied by a plant species across Germany (www.floraweb.de). Plant height (m) was extracted from TRY and LEDA data bases. A full description of the methods related to the plant traits can be found in the original article.
In order to build the insect-plant association dataset, we departed from the plant species list contained in the taxonomic reference database for Germany (Jansen & Dengler, 2008. urn:nbnhebis:30:3-449555). The species richness of insect herbivores associated with each plant was obtained by searching literature and databases. The initial species list of insects for the compilation was obtained in the Fauna Europaea web service (https://fauna-eu.org/), considering both phytophagous and xylophagous records, except for Coleoptera that was obtained from the Palaearctic Catalogue (https://weevil.myspecies.info/content/palaearctic-catalogue). Records of interactions were found on monographs, papers and online resources for host-plant records. Insect records for a given host were accepted if they consumed any plant part as a larva or in the adult phase, such as leaves, stems, branches, trunk, roots, flowers and seeds. Valid records included only plants identified until the species level. Infra-species plant categories were amalgamated and hybrids were excluded. Plant names were standardized according to the World Flora Online (2024. http:// www.worldfloraonline.org). The complete list of literature sources used in this compilation is found in Appendix S1 of the original article.
The material deposit here includes an R project with the data and R scripts for cleaning up and organize the data and perform all analyses.
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Related works
- Is source of
- 10.5061/dryad.73n5tb3c9 (DOI)