Dynamics of Copy Number Variation in Host Races of the Pea Aphid

Abstract

Copy number variation (CNV) makes a major contribution to overall genetic variation and is suspected to play an important role in adaptation. However, aside from a few model species, the extent of CNV in natural populations has seldom been investigated. Here, we report on CNV in the pea aphid Acyrthosiphon pisum, a powerful system for studying the genetic architecture of host-plant adaptation and speciation thanks to multiple host races forming a continuum of genetic divergence. Recent studies have highlighted the potential importance of chemosensory genes, including the gustatory and olfactory receptor gene families (Gr and Or, respectively), in the process of host race formation. We used targeted resequencing to achieve a very high depth of coverage, and thereby revealed the extent of CNV of 434 genes, including 150 chemosensory genes, in 104 individuals distributed across eight host races of the pea aphid. We found that CNV was widespread in our global sample, with a significantly higher occurrence in multigene families, especially in Ors. We also observed a decrease in the gene probability of being completely duplicated or deleted (CDD) with increase in coding sequence length. Genes with CDD variants were usually more polymorphic for copy number, especially in the P450 gene family where toxin resistance may be related to gene dosage. We found that Gr were overrepresented among genes discriminating host races, as were CDD genes and pseudogenes. Our observations shed new light on CNV dynamics and are consistent with CNV playing a role in both local adaptation and speciation.

Recurrent specialization on a toxic fruit in an island Drosophila population

“…Second, our most extreme population genetic differentiation signals did not center on obvious attraction-related genes such as olfactory or gustatory receptors, which might be expected if selection acted on standing genetic variation present in the colonizing population (46,47). Indeed, none of the largest peaks contained any member of the chemosensory gene families whose rapid evolution and turnover are associated with ecological specialization in drosophilids and other insects (7,12,16,22,45). Because a minority of mainland flies visited noni in our experiment, it may be worth testing whether standing genetic variation exists for this trait ( Fig.…”

“…Hungate et al (19) hypothesized that olfactory attraction might have evolved first from recessive alleles segregating in the ancestral range, such as loss-of-function mutations at olfaction-related genes (7,12,15,45). Such attraction would yield strong selection for tolerance alleles, which may often be dominant (13,14) and may originate from new mutations or rare variants in the ancestral populations.…”

“…For example, several unrelated flowering plants produce cardenolides that block activity of the ion gradient regulating enzyme (Na + +K + )ATPase in insects, but identical cardenolideresistant amino acid substitutions in this enzyme have independently arisen in beetles, butterflies, flies, and aphids specializing on such plants (4). Recent genomic studies have focused on parallel dietary shifts in early-diverging ecological races, pointing to a substantial degree of common molecular mechanisms (5)(6)(7)(8). However, at this evolutionary scale, detailed population genetic analyses would be required to distinguish convergent evolution due to adaptive introgression versus selection on independent mutations.…”

Genomics of local adaptation with gene flow

“…), cichlids (Fan & Meyer ), pea aphids (Duvaux et al . ), and monkeyflowers Mimulus guttatus (Flagel et al . ).…”

Adding Complexity to Complexity: Gene Family Evolution in Polyploids

“…An added complication for these types of gene families is that copy number can be variable even among individuals within a species (e.g., Mable et al, 2015), meaning that genome references will not always include the full complement of copies. Copy number variation has been linked to disease severity in humans (Beckmann et al, 2007;Wheeler et al, 2008) and adaptive processes in other organisms (Saintenac et al, 2011;Zmienko et al, 2014;Duvaux et al, 2015;Hull et al, 2017) but methods that can reliably distinguish between lack of coverage and variation in presence of a particular gene copy are required to fully evaluate the evolutionary significance of presence/absence polymorphisms following gene duplication.…”