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