Behavioral evolution accompanying host shifts in cactophilic Drosophila larvae

Abstract

For plant utilizing insects, the shift to a novel host is generally accompanied by a complex set of phenotypic adaptations. Many such adaptations arise in response to differences in plant chemistry, competitive environment, or abiotic conditions. One less well‐understood factor in the evolution of phytophagous insects is the selective environment provided by plant shape and volume. Does the physical structure of a new plant host favor certain phenotypes? Here, we use cactophilic Drosophila, which have colonized the necrotic tissues of cacti with dramatically different shapes and volumes, to examine this question. Specifically, we analyzed two behavioral traits in larvae, pupation height, and activity that we predicted might be related to the ability to utilize variably shaped hosts. We found that populations of D. mojavensis living on lengthy columnar or barrel cactus hosts have greater activity and pupate higher in a laboratory environment than populations living on small and flat prickly pear cactus cladodes. Crosses between the most phenotypically extreme populations suggest that the genetic architectures of these behaviors are distinct. A comparison of activity in additional cactophilic species that are specialized on small and large cactus hosts shows a consistent trend. Thus, we suggest that greater motility and an associated tendency to pupate higher in the laboratory are potential larval adaptations for life on a large plant where space is more abundant and resources may be more sparsely distributed.

Positive selection at sites of chemosensory genes is associated with the recent divergence and local ecological adaptation in cactophilic Drosophila

“…1 ). All stocks were maintained in 8-dram vials with banana-molasses media [ 66 ] in a 25°C incubator on a 14:10 h light:dark cycle.…”

Assessing the Architecture ofDrosophila mojavensisLocomotor Evolution with Bulk Segregant Analysis

“…We utilized single isofemale lines of genome sequenced D. mojavensis from Santa Catalina Island (Drosophila 12 Genomes Consortium 2007) and Guaymas, Sonora, Mexico (Allan and Matzkin 2019) in the laboratory. These populations were selected as having the lowest (Catalina Island) and highest (Sonora) larval speed among the four D. mojavensis populations (Coleman et al 2018), allowing us to maximize the variance in the trait of interest. Additionally, limiting the number of parental genotypes used for a crossing design increases the ability to detect the effects of rare variants (Morozova et al 2015).…”

“…Beyond host plant, further climatic variables, notably temperature and humidity, differ between populations. Thus, the radiation of D. mojavensis into four host populations might potentially be linked to strong environmental selection on a wide array of behavioral traits, and behavioral evolution has been demonstrated for host preference (Newby and Etges 1998; Date et al 2013; 2017; Crowley-Gall et al 2016), courtship behavior (Etges et al 2006) and larval behavior (Coleman et al 2018). Here, we examine locomotor behavior, which displays large, heritable differences across populations (Coleman et al 2018).…”

“…Thus, the radiation of D. mojavensis into four host populations might potentially be linked to strong environmental selection on a wide array of behavioral traits, and behavioral evolution has been demonstrated for host preference (Newby and Etges 1998; Date et al 2013; 2017; Crowley-Gall et al 2016), courtship behavior (Etges et al 2006) and larval behavior (Coleman et al 2018). Here, we examine locomotor behavior, which displays large, heritable differences across populations (Coleman et al 2018). Although it is not clear what the functional consequences or adaptive value of locomotor variation may be in D. mojavensis larvae, we have hypothesized that this may be a foraging related trait, as thought for similar phenotypic variation in D. melanogaster larvae (Sokolowski 1980).…”

Chromosome-level hybrid de novo genome assemblies as an attainable option for non-model organisms

“…There is a constantly increasing panel of tools to assemble reads and polish genome assemblies. 49 molasses medium (Coleman, Benowitz, Jost & Matzkin, 2018) with 125 µg/ml ampicillin and 12.5 76 µg/ml tetracycline to reduce bacteria contamination of the sequencing data. The sequencing 77 methods for short-read data (paired ends and mate pairs) have been described in Allan & Matzkin 78 (2019).…”