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

Dı́az, Fernando; Allan, Carson W.; Matzkin, Luciano M.

doi:10.1186/s12862-018-1250-x

Cited by 7 publications

(9 citation statements)

References 96 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…These chemical differences have shaped the feeding and oviposition behavior of flies as has been shown by the exposure of adults to cactus volatiles [100–102]. Recent analysis of populations differentiation in odorant and gustatory receptors have shown that unlike what might be initially predicted a number of the changes in these receptors suggests that effects at the level of signal transduction in addition to odorant recognition [103]. Further functional analysis is needed to better understand the evolution and functional changes of chemosensory pathways associated with the adaptation to necrotic cacti.…”

Section: Discussionmentioning

confidence: 99%

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

Allan

Matzkin

2019

BMC Genomics

Self Cite

View full text Add to dashboard Cite

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.

show abstract

Section: Discussionmentioning

confidence: 99%

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

Allan

Matzkin

2019

BMC Genomics

Self Cite

View full text Add to dashboard Cite

show abstract

“…Insect chemosensory gene families exhibit rapid evolutionary rates (Sánchez-Gracia et al, 2009;Brand et al, 2015;Diaz et al, 2018;Robertson, 2019). The size of the OBP family, i.e., the number of copies, varies widely across insect groups, including Drosophila (Vieira and Rozas, 2011).…”

Section: Introductionmentioning

confidence: 99%

“…Ecological adaptation is not only expected to affect GR but may also trigger adaptive divergence between ortholog CSP. Indeed, there is evidence of positive selection shaping the evolution of chemosensory genes between recently diverged ecologically different species (Kulmuni et al, 2013;Diaz et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Evolution of the odorant-binding protein gene family in Drosophila

et al. 2022

View full text Add to dashboard Cite

Odorant-binding proteins (OBPs) are encoded by a gene family involved in the perception of olfactory signals in insects. This chemosensory gene family has been advocated as a candidate to mediate host preference and host shifts in insects, although it also participates in other physiological processes. Remarkable differences in the OBP gene repertoire have been described across insect groups, suggesting an accelerated gene turnover rate. The genus Drosophila, is a valuable resource for ecological genomics studies since it comprises groups of ecologically diverse species and there are genome data for many of them. Here, we investigate the molecular evolution of this chemosensory gene family across 19 Drosophila genomes, including the melanogaster and repleta species groups, which are mostly associated with rotting fruit and cacti, respectively. We also compared the OBP repertoire among the closely related species of the repleta group, associated with different subfamilies of Cactaceae that represent disparate chemical challenges for the flies. We found that the gene family size varies widely between species, ranging from 39 to 54 candidate OBPs. Indeed, more than 54% of these genes are organized in clusters and located on chromosomes X, 2, and 5, with a distribution conserved throughout the genus. The family sizes in the repleta group and D. virilis (virilis-repleta radiation) were smaller than in the melanogaster group. We tested alternative evolutionary models for OBP family size and turnover rates based on different ecological scenarios. We found heterogeneous gene turnover rates (GR) in comparisons involving columnar cactus specialists, prickly pear specialists, and fruit dwellers lineages, and signals of rapid molecular evolution compatible with positive selection in specific OBP genes. Taking ours and previous results together, we propose that this chemosensory gene family is involved in host adaptation and hypothesize that the adoption of the cactophilic lifestyle in the repleta group accelerated the evolution of members of the family.

show abstract

“…Several studies have shown the importance of positive selection in the evolution of multigene families, especially in chemosensory genes such as ORs and GRs ( McBride et al 2007 ; Smadja et al 2009 ). Positively selected chemoreceptors may be linked to adaptation in Drosophila species ( Hickner et al 2016 ; Diaz et al 2018 ). In the pea aphid, signatures of selection have been identified in chemosensory genes, including GRs and ORs, which may be implicated in the divergence of pea aphid host races.…”

Section: Resultsmentioning

confidence: 99%

Spodoptera littoralis genome mining brings insights on the dynamic of expansion of gustatory receptors in polyphagous noctuidae

Meslin

Mainet

Montagné

et al. 2022

G3 Genes|Genomes|Genetics

View full text Add to dashboard Cite

The bitter taste, triggered via gustatory receptors, serves as an important natural defense against the ingestion of poisonous foods in animals, and the increased host breadth is usually linked to an increase in the number of gustatory receptor genes. This has been especially observed in polyphagous insect species, such as noctuid species from the Spodoptera genus. However, the dynamic and physical mechanisms leading to these gene expansions and the evolutionary pressures behind them remain elusive. Among major drivers of genome dynamics are the transposable elements but, surprisingly, their potential role in insect gustatory receptor expansion has not been considered yet. In this work, we hypothesized that transposable elements and possibly positive selection would be involved in the highly dynamic evolution of gustatory receptor in Spodoptera spp. We first sequenced de novo the full 465 Mb genome of S. littoralis, and manually annotated the main chemosensory genes, including a large repertoire of 373 gustatory receptor genes (including 19 pseudogenes). We also improved the completeness of S. frugiperda and S. litura gustatory receptor gene repertoires. Then, we annotated transposable elements and revealed that a particular category of class I retrotransposons, the SINE transposons, was significantly enriched in the vicinity of gustatory receptor gene clusters, suggesting a transposon-mediated mechanism for the formation of these clusters. Selection pressure analyses indicated that positive selection within the gustatory receptor gene family is cryptic, only 7 receptors being identified as positively selected. Altogether, our data provide a new good quality Spodoptera genome, pinpoint interesting gustatory receptor candidates for further functional studies and bring valuable genomic information on the mechanisms of gustatory receptor expansions in polyphagous insect species.

show abstract

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

Cited by 7 publications

References 96 publications

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

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

Evolution of the odorant-binding protein gene family in Drosophila

Spodoptera littoralis genome mining brings insights on the dynamic of expansion of gustatory receptors in polyphagous noctuidae

Contact Info

Product

Resources

About