Phylogenomics provides insights into the evolution of cactophily and host plant shifts inDrosophila

Abstract

Cactophilic species of the Drosophila buzzatii cluster (repleta group) comprise an excellent model group to investigate genomic changes underlying adaptation to extreme climate conditions and host plants. In particular, these species offer a subject to study the transition from chemically simpler breeding sites (like prickly pears of the genus Opuntia) to chemically more complex hosts (columnar cacti). Here, we report four highly contiguous genome assemblies of three species of the buzzatii cluster. Based on this genomic data and inferred phylogenetic relationships, we identified candidate taxonomically restricted genes (TRGs) likely involved in the evolution of cactophily and cactus host specialization in internal branches of the subgenus Drosophila. Functional enrichment analyses of TRGs within the buzzatii cluster identified genes involved in detoxification, water preservation, immune system response, anatomical structure development, and morphogenesis. In contrast, processes that regulate responses to stress, as well as the metabolism of nitrogen compounds, transport, and secretion were found in the set of species that are columnar cacti dwellers. These findings are in line with the hypothesis that those genomic innovations brought about instrumental mechanisms underlying adaptation in a group of species that speciated in the arid regions of South America.

Evolution of the odorant-binding protein gene family in Drosophila

“…Protein sequences encoded by single-copy genes were employed to build a species tree that showed the same topology as in recent phylogenomic studies of the repleta group (Moreyra et al, 2022) and the buzzatii cluster (Hurtado et al, 2019). Our estimation of GR using the BDI model, suggests an expansion of the OBP family in Drosophila.…”

“…Even though the range of variation of the OBP repertoire in Drosophilidae is not as wide as in other Dipteran families, we detected intra-specific variation within D. koepferae. Recent phylogenomic studies revealed that Bolivian and Argentinian D. koepferae diverged 0.3-0.7 My ago according to genomic data (Moreyra et al, 2019(Moreyra et al, , 2022. These currently allopatric populations are distributed in a geographic area that has been exposed to paleoclimatic changes that deeply affected the distribution of cacti.…”

“…For each analyzed species, BITACORA requires the genome, its annotation in General Feature Format (GFF file), and the reference proteome. All these files were obtained from the National Center for Biotechnology Information (NCBI) (Sayers et al, 2021) and FlyBase (Larkin et al, 2021), except for species of the buzzatii cluster consisting of two strains of D. koepferae (Fontdevila and Wasserman) derived from collections in Argentina (A) and Bolivia (B), D. buzzatii (Patterson and Wheeler), D. antonietae (Tidon-Sklorz and Sene), and D. borborema (Vilela and Sene); which were recently reported in Moreyra et al (2022) (Supplementary Table 1). We used the BITACORA pipeline to perform two rounds of similarity-based searches with BLAST v. 2.9.0-2 (Camacho et al, 2009) andHMMER v3.3 (Eddy, 2011) as recommended in Vizueta et al (2020a).…”

“…D. buzzatii is denoted as a cactus generalist, although a high preference for prickly pear-type hosts has been reported. Divergence times for species of the repleta group were obtained from Moreyra et al (2022) and for the other species from the Timetree database (Kumar et al, 2017).…”

“…It includes more than 100 species, most adapted to a cactophilic lifestyle, i.e., they use necrotic cacti as breeding, mating, and feeding sites (Oliveira et al, 2012;Jezovit et al, 2017;O'Grady and DeSalle, 2018a). Within this group, the genomes of several species have been sequenced: D. hydei (Rane et al, 2019), D. mojavensis, D. arizona, and D. navojoa (mojavensis cluster, mulleri complex) (Clark et al, 2007;Sanchez-Flores et al, 2016), and D. buzzatii, D. borborema, D. koepferae, and D. antonietae (buzzatii cluster, mulleri complex) (Guillén et al, 2014;Rane et al, 2019;Moreyra et al, 2022). Ecological specialization and resource use have been advocated as key aspects in the evolution and diversification of both the mojavensis and the buzzatii clusters (Matzkin, 2014;Etges, 2019;Hasson et al, 2019;Markow, 2019).…”