Reproductive capacity evolves in response to ecology through common developmental mechanisms in Hawai’ianDrosophila

Abstract

30Lifetime reproductive capacity, or the total number of offspring that an individual can give rise 31 to in its lifetime, is a fitness component critical to the evolutionary process. In insects, female 32 reproductive capacity is largely determined by the number of ovarioles, the egg-producing 33 subunits of the ovary. Recent work has provided insights into the genetic and environmental 34 control of ovariole number in Drosophila melanogaster. However, whether regulatory 35 mechanisms discovered under laboratory conditions also explain evolutionary variation in 36 natural populations is an outstanding question. Here we report, for the first time, insights into the 37 mechanisms regulating ovariole number and its evolution among Hawai'ian Drosophila, a large 38 adaptive radiation of fruit flies in which the highest and lowest ovariole numbers of the genus 39 have evolved within 25 million years. Using phylogenetic comparative methods, we show that 40 ovariole number variation among Hawai'ian Drosophila is best explained by adaptation to 41 specific oviposition substrates. Further, we show that evolution of oviposition on ephemeral egg-42 laying substrates is linked to changes the allometric relationship between body size and ovariole 43 number. Finally, we provide evidence that the developmental mechanism principally responsible 44 for controlling ovariole number in D. melanogaster also regulates ovariole number in natural 45 populations of Hawai'ian drosophilids. By integrating ecology, organismal growth, and cell 46 behavior during development to understand the evolution of ovariole number, this work connects 47 the ultimate and proximate mechanisms of evolutionary change in reproductive capacity. 48 49

Topology-driven protein-protein interaction network analysis detects genetic sub-networks regulating reproductive capacity

“…The D. melanogaster ovary is a commonly studied model for organogenesis (Chen et al, 2001;Godt and Laski, 1995;Lobell et al, 2017;Sarikaya and Extavour, 2015), stem cell maintenance (Gilboa, 2015) and interactions of development and ecology (Cohet and David, 1978;Hodin and Riddiford, 2000a;Klepsatel et al, 2013a;Sarikaya et al, 2019). Nevertheless, our understanding of the genetic mechanisms that regulate these processes remains fragmentary.…”

“…In these organs, the effects of multiple genes and the environment combine to produce a quantitative phenotype: a species-specific average number of eggproducing ovarian tubes called ovarioles. Fruit fly ovaries can contain as few as one and as many as 50 ovarioles per ovary, depending on the species (Kambysellis and Heed, 1971;King, 1970;Markow et al, 2009;Sarikaya et al, 2019), with each ovariole capable of producing eggs.…”

“…While ovariole number within a species can vary across temperatures (Azevedo et al, 1996), altitudinal and latitudinal clines (Capy et al, 1994;David and Bocquet, 1975), under constant environmental conditions ovariole number is highly stereotypic (Capy et al, 1993;Klepsatel et al, 2013a;R'Kha et al, 1991;R´kha et al, 1997). The reproducibility of ovariole number thus indicates a strong genetic component (Sarikaya et al, 2019). Genome wide association studies and quantitative trait locus mapping have demonstrated that the ovariole number is a highly polygenic trait (Bergland et al, 2008;Lobell et al, 2017;Orgogozo et al, 2006;Wayne et al, 2001;Wayne et al, 1997;Wayne and McIntyre, 2002).…”

“…In these organs, the effects of multiple genes and the environment combine to produce a quantitative phenotype: a species-specific average number of egg-producing ovarian tubes called ovarioles. Fruit fly ovaries can contain as few as one and as many as 50 ovarioles per ovary, depending on the species ( Kambysellis and Heed, 1971 ; King, 1970 ; Markow et al, 2009 ; Sarikaya et al, 2019 ), with each ovariole capable of producing eggs. Ovariole number, therefore, may affect the reproductive fitness of Drosophila species by determining the potential of an adult female to produce eggs ( Klepsatel et al, 2013b ; R' kha et al, 1997 ).…”