Natural populations of Hawaiian Drosophila  – which we have to go to Hawaii to find! – are a promising study system to understand rapid evolutionary changes in reproductive life history.

Insect ovaries are subdivided into egg-producing units called ovarioles, which range from 1 to over 100 across Drosophila species, and whose mean number can positively predict egg-laying capacity. Observing that similar ovariole numbers have evolved independently in distinct Drosophila lineages, we asked whether this convergent evolution was due to changes in the same or different developmental processes. We discovered that similar ovariole numbers were achieved via distinct developmental mechanisms in different lineages. By using our developmental data to re-examine previous quantitative genetic data on ovariole number variation, we uncovered genetic regulators of ovariole number including the Drosophila Insulin-like receptor (InR), Hippo signaling pathway members, and the transcription factor bric-a-brac. We showed that the developmental processes underlying ovariole number are genetically separable.

In our work on the molecular mechanisms of interspecies ovariole number variation, we have found that evolution of insulin signaling underlies not only divergence, but also differential plasticity of ovariole number between D. melanogaster and D. sechellia. Our results suggest how differential phenotypic plasticity may explain observed patterns of ovariole number variation in different insects.

To extend our findings from the lab to the wild, we also study natural Drosophila populations. Of the roughly 4000 described Drosophila species, nearly 1000 of them evolved in the Hawaiian Islands over the last 20-25 million years. In adapting to the volcanic Hawaiian landscape, they have evolved more ecological, behavioural, morphological and reproductive diversity than all other Drosophila species combined. Inspired by the Hawaiian Drosophila Project of the 1960s, and in collaboration with some of its original participants and their successors, we aim to further the study of Hawaiian Drosophila as a powerful study system for understanding the mechanistic basis of explosive adaptive radiations.

We have successfully collected individuals from all major clades of Hawaiian Drosophila (examples shown in movie above), and determined that evolutionary variation in the cellular mechanism that controls ovariole number in D. melanogaster, can explain species-specific variation in the wild even in species with many more or fewer ovarioles than D. melanogaster. We also find that the phylogenetic distribution of ovariole number is best explained by adaptation to distinct habitats, implying that the developmental mechanisms regulating ovariole number may have been targets of natural selection, potentially allowing adaptation of fecundity to unique ecologies.

Going forward, we wish to address how the integration of environment, hologenome and development determine the nature of variation available in the germ line at each generation.

References

Gene protein sequence evolution can predict the rapid divergence of ovariole numbers in Drosophila. C.A. Whittle, C. G. Extavour bioRxiv, 556080 (2024). [PubMed]
The evolution of ovary-biased gene expression in Hawaiian Drosophila. Church, S.H., Munro, C., Dunn, C. and Extavour C.G. PLoS Genetics (in press), 19(1): e1010607 (2023). [PubMed]
Phylotranscriptomics Reveals Discordance in the Phylogeny of Hawaiian Drosophila and Scaptomyza (Diptera: Drosophilidae). Church, S.H. and Extavour C.G. Molecular Biology and Evolution, 39(3): msac012 (2022). [PubMed]
Repeated loss of variation in insect ovary morphology highlights the role of development in life-history evolution. Church, S.H., de Medeiros, B.A.S., Donoughe, S.D., Marquez Reyes, N.L. and Extavour, C.G. Proceedings of the Royal Society - Part B, 288(1950):20210150 (2021). [PubMed]
Null hypotheses for developmental evolution. Church, S.H. and Extavour, C.G. Development, 147(8):dev178004 (2020). [PubMed]
Reproductive Capacity Evolves in Response to Ecology through Common Changes in Cell Number in Hawaiian Drosophila. Sarikaya, D.P.*, Church, S.H., Lagomarsino L.P., Magnacca K.M., Montgomery S.L., Price D.P., Kaneshiro K.Y. and Extavour C.G.* Current Biology, 29(11): 1877-1884 (2019).

Related Media: [PubMed]
Ancestral and offspring nutrition interact to affect life history traits in Drosophila melanogaster. Deas, J.B.*, Blondel, L. and Extavour, C.G.* Proceedings of the Royal Society B, 286(1897):20182778 (2019). [PubMed]
The significance and scope of evolutionary developmental biology: a vision for the 21st century. Moczek, A., Sears, K., Stollewerk, A., Wittkopp, P., Diggle, P., Dworkin, I., Ledon-Rettig, C., Matus, D., Roth, S., Abouheif, E., Brown, F. Chiu, C.-H., Cohen, C.S., De Tomaso, T., Gilbert, S., Hall, B., Love, A., Lyons, D., Sanger, T., Smith, J., Specht, C., Vallejo-Marin, M. and Extavour, C.G. Evolution and Development, 17(3): 198-219 (2015). [PubMed]
Insulin Signaling Underlies Both Plasticity and Divergence of a Reproductive Trait in Drosophila. Green II, D.A. and Extavour, C.G. Proceedings of the Royal Society B: Biological Sciences, 281(1779): 20132673 (2014).

Related Media: [PubMed]
Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila. Green II, D.A. and Extavour, C.G. Developmental Biology, 372(1): 120-130 (2012). [PubMed]
The roles of cell size and cell number in determining ovariole number in Drosophila. Sarikaya, D.P., Belay, A.A., Ahuja, A., Green II, D.A., Dorta, A. and Extavour, C.G. Developmental Biology, 363(1): 279-289 (2012). [PubMed]
Counting in oogenesis. Green, D.A.*, Sarikaya, D.P.* and Extavour, C.G Cell and Tissue Research, 344(2): 207-212 (2011). [PubMed]
Gray Anatomy: phylogenetic patterns of somatic gonad structures and reproductive strategies across the Bilateria. Extavour, C.G Integrative and Comparative Biology, 47(3): 420-426 (2007).

Related Media: [PubMed]