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. 2016 Aug 27;8(8):2493-504.
doi: 10.1093/gbe/evw191.

Weak Polygenic Selection Drives the Rapid Adaptation of the Chemosensory System: Lessons from the Upstream Regions of the Major Gene Families

Pablo Librado  1 , Julio Rozas  2
Affiliations

Weak Polygenic Selection Drives the Rapid Adaptation of the Chemosensory System: Lessons from the Upstream Regions of the Major Gene Families

Pablo Librado et al. Genome Biol Evol. .

Abstract

The animal chemosensory system is involved in essential biological processes, most of them mediated by proteins encoded in multigene families. These multigene families have been fundamental for the adaptation to new environments, significantly contributing to phenotypic variation. This adaptive potential contrasts, however, with the lack of studies at their upstream regions, especially taking into account the evidence linking their transcriptional changes to certain phenotypic effects. Here, we explicitly characterize the contribution of the upstream sequences of the major chemosensory gene families to rapid adaptive processes. For that, we analyze the genome sequences of 158 lines from a population of Drosophila melanogaster that recently colonized North America, and integrate functional and transcriptional data available for this species. We find that both, strong negative and strong positive selection, shape transcriptional evolution at the genome-wide level. The chemosensory upstream regions, however, exhibit a distinctive adaptive landscape, including multiple mutations of small beneficial effect and a reduced number of cis-regulatory elements. Together, our results suggest that the promiscuous and partially redundant transcription and function of the chemosensory genes provide evolutionarily opportunities for rapid adaptive episodes through weak polygenic selection.

Keywords: Drosophila; chemosensory; natural selection; transcription; upstream regions.

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Figures

<sc>Fig</sc>. 1.—
Fig. 1.—
Nucleotide diversity levels (π) at three putatively neutral classes of sites: the 4-fold degenerate sites, the positions 8–30 of short introns (≤65 bp), and 2-kb upstream regions. π was separately computed for all the autosomal and X-linked regions.
<sc>Fig</sc>. 2.—
Fig. 2.—
The unfolded site frequency spectrum summarizing the proportion of biallelic sites with a given number of derived alleles. It was calculated from the positions 8–30 of all short introns (≤65 bp) across the autosomal and X chromosomes.
<sc>Fig</sc>. 3.—
Fig. 3.—
Distribution of fitness effects of new deleterious mutations in autosomal chromosomes, partitioned into four categories: nearly neutral (0 < −Nes < 1), slightly deleterious (1 < −Nes < 10), mildly deleterious (10 < −Nes < 100) and strongly deleterious (100 < −Nes).
<sc>Fig</sc>. 4.—
Fig. 4.—
Top 25 GO categories according to their median pa values. In bold, the category “detection of chemical stimulus involved in sensory perception”, which comprises all surveyed chemosensory families. It ranks in position 17 (out of 727 GO terms with >20 members), approximately representing the top-2%.
<sc>Fig</sc>. 5.—
Fig. 5.—
Association between the frequencies of derived mutations and the transcriptional fold change they induce (EIR; see “Materials and Methods” section). Red and grey points depict SNPs in chemosensory and nonchemosensory upstream regions, respectively. eQTLs at chemosensory upstream regions (red) producing a significant transcriptional change are labeled with the corresponding gene name. The background shaded areas define the categories for extreme (>0.9, or < 0.1) and intermediate (from 0.4 to 0.6) derived allele frequencies.
See this image and copyright information in PMC

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