Comparative phylogeogeography of South African chafers (Coleoptera, Scarabaeidae) -inferring the evolution of diversity in a biodiversity hotspot.
Final Report Abstract
1) Our study settled for the first time a detailed historical and evolutionary background for the mode of evolutionary diversification of all major chafer lineages (Scarabaeoidea). We build a detailed timecalibrated tree based on four DNA markers and on the conservatively evaluated fossil record. The phylogeny revealed multiple origins of coprophagy, phytophagy, and anthophagy and widely confirmed a Jurassic origin of Scarabaeoidea crown group, while crown groups of phytophagous lineages began to radiate first after the rise of angiosperms, followed by the later diversification of coprophagous lineages. Pollen feeding arose even later. The clear time lag between the origins of herbivores and coprophages suggests an evolutionary path driven by the angiosperms that first favoured the herbivore fauna (mammals, insects) followed by a secondary radiation of dung feeders. 2) This historical background was studied more in detail for the model group Sericini for which a West Gondwanan origin (112 Ma) was reconstructed. Vicariance in the tribe’s earliest history separated Neotropical and Old World lineages, whereas subsequent lower Cretaceous biogeography of the tribe was characterized by repeated migrations out of Africa, resulting in the colonization of Eurasia and Madagascar. Diversification dynamics revealed three independent shifts to increased speciation rates: in African ant-adapted Trochalus, Oriental Tetraserica, and Asian and African Sericina. Southern Africa was identified as cradle and refuge of Sericini which retained many old lineages that portray the evolution of the African Sericini fauna as a series of taxon pulses. 3) DNA-based species delimitation using Cox1 on southern African Sericini confirmed that DNA-based species delimitation may be compromised by limited sampling and species rarity, including “singletons” which hampers estimates of intra- versus interspecies evolutionary processes. By extended sampling of the empirical data and tree simulations we explored empirical generalities of DNA-based species delimitation in this regard. We found that low sampling may be compensated for by “clade addition” of lineages outside of the focal group. Low performance of poorly sampled trees (as with GMYC modelling) is not due to high proportions of singletons per se, but due to variable effective population size (Ne) which is exacerbated by variable species abundances. Hence, low sampling success and rarity of species affect the power of coalescent-based species delimitation (e.g., GMYC) only if they reflect great differences in Ne among species. 4) Furthermore, we investigated evolutionary patterns of body shape in the highly diverse phytophagous chafers (Scarabaeidae) which feed polyphagously on angiosperms. Because reasons of successful diversification of scarab chafers are largely unknown, we used a multivariate analysis on linear measurements of body morphology to infer patterns of morphospace covariation and divergence. Different feeding types resulted to be not distinguishable in morphospace which was largely attributed to large occupancy of the morphospace of some feeding types and to multiple convergences of feeding behaviour (e.g., anthophagy). Between some sister clades strong divergences occurred, while others showed convergent shape evolution. Low correlation between molecular and morphological rates, including significant rate shifts for some lineages, indicated directed selection within feeding types. 5) We investigated the question whether asymmetry might facilitate or accelerate morphological divergence of genitalia between species. This hypothesis was tested in the chafer genus Schizonycha which comprises species with symmetric and asymmetric male genitalia. Morphometric analyses on copulation organs of 34 species were conducted in context of their phylogeny, inferred from mitochondrial and nuclear ribosomal DNA sequence data. We found a continuous transition in the degree of asymmetry among the investigated species and multiple origins of asymmetry including high evolutionary plasticity of asymmetry. Since no significant correlation between evolutionary rates of shape divergence and the degree of asymmetry was found, we concluded that asymmetric genitalia in Schizonycha do not increase the rate of genital shape divergence. 6) We demonstrated that continuous morphological trait data can be extremely valuable in assessing competing hypotheses to species delimitation. Defining species can be challenging, especially during the earliest stages of speciation, when phylogenetic inference and delimitation methods may be compromised by incomplete lineage sorting or secondary gene flow, as encountered in Pleophylla. The inclusion of morphological data in an integrative Bayesian framework can improve the resolution of inferred species units. However, we also demonstrated that this approach is extremely sensitive to guide tree and prior parameter choice. 7) Finally, we used an integrated approach of population-level phylogeography and climatic niche modeling of forest associated Pleophylla chafers to assess connectivity and potential extent of forest habitats since the last glacial maximum. Current and past species distribution models supported a much wider potential current extension of forests based on climatic data. Considerable genetic admixture of mitochondrial and nuclear DNA among many populations and an increase of mean population mutation rate in Extended Bayesian Skyline Plots of all species indicated more extended or better connected forests in the recent past (< 5 kya). Genetic isolation of certain populations and landscape connectivity statistics and models of current and near future habitat conditions suggest strong loss of habitat connectivity.
Publications
- (2014) Building the Coleoptera tree-of-life for >8000 species: composition of public DNA data and fit with Linnaean classification. Systematic Entomology 39: 97–110
Bocak, L., Barton, C., Crampton-Platt, A., Chesters, D., Ahrens, D., Vogler, A.P.
(See online at https://doi.org/10.1111/syen.12037) - (2014) The evolution of morphospace in phytophagous scarab chafers: no competition - no divergence? Plos One 9 (5): e98536
Eberle, J., Myburgh, R. & Ahrens, D.
(See online at https://doi.org/10.1371/journal.pone.0098536) - The evolution of scarab beetles tracks the sequential rise of angiosperms and mammals. Proceedings of the Royal Society B 2014 281
Ahrens, D., Schwarzer, J. & Vogler, A.P.
(See online at https://doi.org/10.1098/rspb.2014.1470) - (2015) Asymmetry in genitalia does not increase the rate of their evolution. Molecular Phylogenentics and Evolution 93: 180–187
Eberle, J., Walbaum, W., Fabrizi, S., Ahrens, D.
(See online at https://doi.org/10.1016/j.ympev.2015.08.005) - (2015) Taxonomic utility of female copulation organs in Sericini chafers (Coleoptera, Scarabaeidae), with special reference to asymmetry. Contributions to Zoology 84 (2) 167-178
Özgül-Siemund, A. & Ahrens, D.
- (2016) Bayesian species delimitation in Pleophylla chafers (Coleoptera) – the importance of prior choice and morphology. BMC Evolutionary Biology 16:94
Eberle, J., Warnock, R.C.M., Ahrens, D.
(See online at https://doi.org/10.1186/s12862-016-0659-3) - (2016) Rarity and incomplete sampling in DNA-based species delimitation. Systematic Biology
Ahrens, D., Fujisawa, T., Krammer, H.-J., Eberle, J., Fabrizi, S. & Vogler, A.P.
(See online at https://doi.org/10.1093/sysbio/syw002) - (2016a) A historical biogeography of megadiverse Sericini – another story “out of Africa”? Cladistics; published online: 19 Apr 2016
Eberle, J., Fabrizi, S., Lago, P. & Ahrens, D.
(See online at https://doi.org/10.1111/cla.12162)
