Genomic analysis of the four ecologically distinct cactus host populations of Drosophila mojavensis

Abstract

BackgroundRelationships between an organism and its environment can be fundamental in the understanding how populations change over time and species arise. Local ecological conditions can shape variation at multiple levels, among these are the evolutionary history and trajectories of coding genes. This study examines the rate of molecular evolution at protein-coding genes throughout the genome in response to host adaptation in the cactophilic Drosophila mojavensis. These insects are intimately associated with cactus necroses, developing as larvae and feeding as adults in these necrotic tissues. Drosophila mojavensis is composed of four isolated populations across the deserts of western North America and each population has adapted to utilize different cacti that are chemically, nutritionally, and structurally distinct.ResultsHigh coverage Illumina sequencing was performed on three previously unsequenced populations of D. mojavensis. Genomes were assembled using the previously sequenced genome of D. mojavensis from Santa Catalina Island (USA) as a template. Protein coding genes were aligned across all four populations and rates of protein evolution were determined for all loci using a several approaches.ConclusionsLoci that exhibited elevated rates of molecular evolution tend to be shorter, have fewer exons, low expression, be transcriptionally responsive to cactus host use and have fixed expression differences across the four cactus host populations. Fast evolving genes were involved with metabolism, detoxification, chemosensory reception, reproduction and behavior. Results of this study give insight into the process and the genomic consequences of local ecological adaptation.

Mate discrimination among subspecies through a conserved olfactory pathway

“…Phylogenetic analysis. The phylogenetic relationship among the four D. mojavensis subspecies and D. melanogaster was determined using the recent genomic analysis of D. mojavensis (Allan and Matzkin, 2019) and the D. melanogaster FlyBase assembly (FB2019_04). The BUSCO application (Waterhouse et al, 2018) was ran using the Diptera dataset (composed of 2,799 loci) for all five genomes and a common set of 2,622 loci was obtained.…”

“…Phylogenetic analyses revealed that the two northern subspecies and the two southern subspecies clustered with each other ( Figure 1B) (Allan and Matzkin, 2019). These closely-related subspecies exhibit many differences in their morphology (Pfeiler et al, 2009), neurophysiological responses (Crowley-Gall et al, 2016;Date et al, 2013;Nemeth et al, 2018), genomic and transcriptomic characteristics (Allan and Matzkin, 2019;Matzkin, 2014;Matzkin and Markow, 2013), and behavioral traits (Newby and Etges, 1998). Experimental reciprocal crosses between these allopatric subspecies resulted in viable fertile offspring, indicating presence of prezygotic isolation mechanisms (Knowles and Markow, 2001;Krebs and Markow, 1989;Markow, 1991;Zouros and Dentremont, 1980).…”

“…baja breed and feed on the organ pipe cactus in the mainland Sonoran Desert and the agria cactus in the Baja California, respectively (Heed, 1978;Ruiz et al, 1990). Phylogenetic analyses revealed that the two northern subspecies and the two southern subspecies clustered with each other ( Figure 1B) (Allan and Matzkin, 2019). These closely-related subspecies exhibit many differences in their morphology (Pfeiler et al, 2009), neurophysiological responses (Crowley-Gall et al, 2016;Date et al, 2013;Nemeth et al, 2018), genomic and transcriptomic characteristics (Allan and Matzkin, 2019;Matzkin, 2014;Matzkin and Markow, 2013), and behavioral traits (Newby and Etges, 1998).…”

“…baja; adapted from (Pfeiler et al, 2009). B, Phylogenetic relationship of D. mojavensis subspecies based on concatenated sequences of 9087 genes available from (Allan and Matzkin, 2019) (See STAR Methods for details). Scale bar for branch length represents the number of substitutions per site.…”

Contributions of cis- and trans-Regulatory Evolution to Transcriptomic Divergence across Populations in the Drosophila mojavensis Larval Brain

“…These host cacti form unique chemical and nutritional environments ( Kircher 1982 ; Starmer and Phaff 1983 ), and detoxification genes in particular have seen substantial expression and coding sequence evolution across these populations ( Matzkin et al. 2006 ; Allan and Matzkin 2019 ). In addition to selection from the host, these populations experience vastly different temperature and humidity regimes, which is expected to generate selection broadly on phenology and organismal physiology ( Matzkin 2014 ).…”