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Somatic Gonad Research

Developmental Mechanisms That Regulate Reproductive Capacity

 

The fitness of an individual depends heavily on the number of offspring produced by that individual. Evolutionary changes in the morphologies and processes that determine the number of offspring can therefore impact fitness, and may be subject to natural selection. We are interested in how reproductive system morphology and function impact reproductive capacity, and how evolutionary changes in gonad development and function may have contributed to changes in reproductive capacity and hence fitness. We study this problem using ovariole number in Drosophilid flies as a model.

All insect ovaries are divided into egg-producing units called ovarioles. Ovariole number is highly variable between species, but highly heritable within species. Ovariole number in some insects also displays phenotypic plasticity, and can be influenced by environmental temperature or larval nutrition. The first step in ovariole morphogenesis in Drosophila is the formation of stacks of eight to ten cells, called terminal filaments, in the anterior of the larval ovary. The number of terminal filaments that form during larval development determines adult ovariole number. This means that to understand the genetic basis of ovariole number, we need to understand the genetic control of terminal filament formation.

 

Dmovary

Drosophila larval ovary showing the positions of terminal filaments (magenta) and apical cells (green). Cell outlines are marked by actin (red) and nuclei by DAPI (cyan).

We have found that the critical parameter that determines terminal filament number (and hence ovariole number) is the number of terminal filament cells. Species-specific ovariole number in Drosophilids can therefore be predicted from the total number of terminal filament cells in a given species. Interestingly, we have shown that temperature-dependent plasticity in ovariole number is not achieved by altering terminal filament cell number, but instead by changes in terminal filament cell sorting during terminal filament formation.

The number of terminal filament cells depends on how many cells are allocated to the somatic gonad primordium during embryogenesis, the proliferation rate of these cells during larval development, and the morphogenetic movements undergone by these cells in late larval life. We have uncovered a novel role for the conserved Hippo pathway, which regulates growth in animals, in the proliferation of all ovarian cell types. However, in the ovary the Hippo pathway appears to operate via distinct downstream signaling pathways in different cells of the same organ. Ongoing and planned projects in this area include further elucidation of the molecular mechanisms of Hippo-mediated ovarian size control, and screens to discover additional genes involved in regulating ovariole number.

References

Green, D.A.*, Sarikaya, D.P.* and Extavour, C.G. Counting in oogenesis. Cell and Tissue Research 344(2): 207-212 (2011) PDF PubMed (* equal author contribution)

Sarikaya, D.P., Belay, A.A., Ahuja, A., Green, D.A., Dorta, A. and Extavour, C.G. The roles of cell size and cell number in determining ovariole number in Drosophila. Developmental Biology 363(1): 279-289 (2012) PDF PubMed

Sarikaya, D.P. and Extavour, C.G. The Hippo pathway regulates coordinated proliferation of somatic and germ cells in the Drosophila ovary. (in preparation)


Developmental Genetic Basis of Ovariole Number Evolution

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 recent 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.

Our current work in this area focuses on identifying the genetic basis of ovariole number variation in African Drosophilids. In addition, we have begun work on the relationship between ecological niche and ovariole number variation in Hawaiian Drosophilids. These Hawaiian fruit flies have extreme ovariole numbers, ranging a full order of magnitude above and below those observed for African fruit flies. Ovariole number is also correlated with the relative abundance of larval nutrition. We are examining the developmental basis of ovariole number determination in this diverse group of species.

References

Green II, D.A., and Extavour, C.G. Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila. Developmental Biology 372(1): 120-130 (2012) PDF PubMed

Green, D.A. and Extavour, C.G. Insulin Signaling Underlies Both Plasticity and Divergence of a Reproductive Trait in Drosophila. Proceedings of the Royal Society B: Biological Sciences doi:10.1098/rspb.2013.2673 published online March 22 (2014) PDF