An amino acid polymorphism in the couch potato gene forms the basis for climatic adaptation in Drosophila melanogaster

Abstract

Diapause is the classic adaptation to seasonality in arthropods, and its expression can result in extreme lifespan extension as well as enhanced resistance to environmental challenges. Little is known about the underlying evolutionary genetic architecture of diapause in any organism. Drosophila melanogaster exhibits a reproductive diapause that is variable within and among populations; the incidence of diapause increases with more temperate climates and has significant pleiotropic effects on a number of life history traits. Using quantitative trait mapping, we identified the RNAbinding protein encoding gene couch potato (cpo) as a major genetic locus determining diapause phenotype in D. melanogaster and independently confirmed this ability to impact diapause expression through genetic complementation mapping. By sequencing this gene in samples from natural populations we demonstrated through linkage association that variation for the diapause phenotype is caused by a single Lys/Ile substitution in one of the six cpo transcripts. Complementation analyses confirmed that the identified amino acid variants are functionally distinct with respect to diapause expression, and the polymorphism also shows geographic variation that closely mirrors the known latitudinal cline in diapause incidence. Our results suggest that a naturally occurring amino acid polymorphism results in the variable expression of a diapause syndrome that is associated with the seasonal persistence of this model organism in temperate habitats.cline ͉ diapause ͉ life history ͉ mapping ͉ tradeoff N atural populations encounter environmental stresses that diminish individual fitness, and these stresses are variable across space and time. It is predicted that the resulting natural selection often leads to a situation in which no genotype has the highest fitness across all environments, and polymorphism is maintained. This concept is pervasive in arguments about the evolution of life history variation and associated genetic tradeoffs (1). However, the expected molecular polymorphism associated with life history tradeoffs and adaptation remains elusive. Although we would expect these phenomena to be universal, the complexities of genetic dissection of such variation suggest that the best opportunity to identify the genetic basis for life history variation lies in the study of the genetic models in their natural populations (2).Drosophila melanogaster is a human commensal that has spread from areas of Sub-Saharan Africa to Europe and Asia, possibly over the last 5,000 to 16,000 years, and into the Western Hemisphere and Australia in the past several hundred years (3-5). This worldwide expansion from the tropics has required adaptation to the pronounced seasonality present in temperate habitats, and there are many examples of both single-gene polymorphism and quantitative trait variation that show geographic patterns associated with the transition from tropical to temperate climates in this species (6, 7). There also is good evidence that D. melanogaster ov...

Dissecting the genetics of longevity inDrosophila melanogaster

“…68 However, a single nucleotide polymorphism at cpo shows strong control over the ability of D. melanogaster to enter diapause. 66 The SNP shows a significant cline in frequency across latitude in the eastern U.S., suggesting a functional response to heterogeneous selection pressure. While neither of these genes have been demonstrated as aging genes in the laboratory, the association of Dp110 with the insulin signaling pathway, a major mediator of lifespan, and the association of both genes with diapause, a process that directly mediates lifespan and is strongly genetically correlated with natural variation in longevity, 64,65 suggests that they may play an important role in determining lifespan phenotypes in wild populations.…”

“…65 QTL and complementation mapping identified couch potato (cpo) as a major determinant of diapause, and consequently as a likely candidate for determining lifespan phenotypes in natural populations. 66 Variation in diapause expression has also been linked to allelic variation at both timeless (tim), a light-dependent component of the circadian like juvenile hormone and ecdysone, which are well-evidenced determinants of insect life history. 37 Mutations that disrupt the ecdysone receptor, EcR, and DTS-3, which is involved in ecdysone biosynthesis, also extend lifespan.…”

Genomic Differentiation Between Temperate and Tropical Australian Populations ofDrosophila melanogaster

“…For major phenotypic variants having a simple genetic basis but no candidate genes, genetic analysis can be used to isolate alternative alleles underlying the phenotypic difference. Examples include diapause variation and foraging behavior in Drosophila melanogaster (Osborne et al 1997;Schmidt et al 2008), traits relating to social behavior and copulatory plug formation in Caenorhabditis elegans (de Bono and Bargmann 1998;Palopoli et al 2008), and several phenotypes in sticklebacks (Colosimo et al 2004;Miller et al 2007;Chan et al 2010). Besides their simple genetics, such biological examples have the advantage that the targeted traits may have plausible connections to fitness variation in nature (though this is not always the case).…”

“…Although circadian rhythm genes are not overrepresented among the F ST outliers, several genes relating to circadian biology are found among the most differentiated 1-kb windows. The cryptochrome gene, which regulates circadian rhythm, is highly differentiated (F ST ¼ 0.30), as are couch potato (F ST ¼ 0.23) and timeless (F ST ¼ 0.20), which have already been implicated in spatially varying selection in D. melanogaster Tauber et al 2007;Schmidt et al 2008). Another interesting candidate is norpA, a phospholipase C gene required for thermal synchronization of the circadian clock (Glaser and Stanewsky 2005).…”

Using Environmental Correlations to Identify Loci Underlying Local Adaptation

“…The study of geographic patterns of genetic variation has a long history, with some of the earliest work on genetic polymorphism being the study of clines in the frequency of cytologically visible inversion polymorphisms (Dobzhansky 1948). Other examples include loci involved in adaptations to high altitude (Storz et al 2007;McCracken et al 2009), pigmentation (Hoekstra et al 2004), and life-history changes (Schmidt et al 2008). One particularly impressive example of adaptive response to selection is provided by the ADH locus in Drosophila melanogaster, alleles of which show a strong gradient with latitude (Berry and Kreitman 1993).…”