Two decades of suspect evidence for adaptive DNA-sequence evolution – Less negative selection misconstrued as positive selection

Abstract

Evidence for biological adaptation is often obtained by studying DNA sequence evolution. Since the analyses are affected by both positive and negative selection, studies usually assume constant negative selection in the time span of interest. For this reason, hundreds of studies that conclude adaptive evolution might have reported false signals caused by relaxed negative selection. We test this suspicion two ways. First, we analyze the fluctuation in population size, N, during evolution. For example, the evolutionary rate in the primate phylogeny could vary by as much as 2000 fold due to the variation in N alone. Second, we measure the variation in negative selection directly by analyzing the polymorphism data from four taxa (Drosophila, Arabidopsis, primates, and birds, with 64 species in total). The strength of negative selection, as measured by the ratio of nonsynonymous/synonymous polymorphisms, fluctuates strongly and at multiple time scales. The two approaches suggest that the variation in the strength of negative selection may be responsible for the bulk of the reported adaptive genome evolution in the last two decades. This study corroborates the recent report 1 on the inconsistent patterns of adaptive genome evolution. Finally, we discuss the path forward in detecting adaptive sequence evolution.

Ancestral transoceanic colonization and recent population reduction in a nonannual killifish from the Seychelles archipelago

“…In agreement with recent findings that positive selection is in general difficult to detect especially in the presence of repeated relaxed purifying selection (Chen et al, 2020), we found weak evidence for positive selection in the golden panchax using both population genetics and phylogenetic methods.…”

“…The relax method relies on fixed differences between species, which probably reflect the selective pressure in a more ancient past. Over a recent time frame, however, population size declined steadily over the past 200,000 generations in most of the golden panchax populations we analysed, probably reflecting the rising sea level and the shrinking island size since the last glacial period (Grant et al, 2012 In agreement with recent findings that positive selection is in general difficult to detect especially in the presence of repeated relaxed purifying selection (Chen et al, 2020), we found weak evidence for positive selection in the golden panchax using both population genetics and phylogenetic methods.…”

Genomics of a killifish from the Seychelles islands supports transoceanic island colonization and reveals relaxed selection of developmental genes

“…In agreement with recent findings that positive selection is in general difficult to detect especially in the presence of repeated relaxed purifying selection (Chen, et al 2020), we found weak evidence for positive selection in the golden panchax using both population genetics and phylogenetic methods.…”

Two decades of suspect evidence for adaptive molecular evolution – Negative selection confounding positive selection signals

“…In Chen et al (2020), the indirect inferences of changes in negative selection through time as a function of Ne changes have been done in several species of primates [55]. Most interesting, by using PSMC, one could take the direct approach to negative selection by calculating Pa/Ps for each time interval.…”

“…In light of the current report, we now outline a path forward that is elaborated in the companion study [55]. In taking the new path, we are concerned with measuring the fluctuation in negative selection without addressing the many factors underlying the fluctuation.…”