Enrichment of Hard Sweeps on the X Chromosome in Drosophila melanogaster

Abstract

The characteristic properties of the X chromosome, such as male hemizygosity and its unique inheritance pattern, expose it to natural selection in a way that can be different from the autosomes. Here, we investigate the differences in the tempo and mode of adaptation on the X chromosome and autosomes in a population of Drosophila melanogaster. Specifically, we test the hypothesis that due to hemizygosity and a lower effective population size on the X, the relative proportion of hard sweeps, which are expected when adaptation is gradual, compared to soft sweeps, which are expected when adaptation is rapid, is greater on the X than on the autosomes. We quantify the incidence of hard versus soft sweeps in North American D. melanogaster population genomic data with haplotype homozygosity statistics and find an enrichment of the proportion of hard versus soft sweeps on the X chromosome compared to the autosomes, confirming predictions we make from simulations. Understanding these differences may enable a deeper understanding of how important phenotypes arise as well as the impact of fundamental evolutionary parameters on adaptation, such as dominance, sex-specific selection, and sex-biased demography.

Enrichment of hard sweeps on the X chromosome compared to autosomes in sixDrosophilaspecies

“…A classic question in evolutionary biology is how the evolution of the X chromosome differs from that of autosomes given the X chromosome's central role in speciation, brain function, fertility, and sexual dimorphism (Rice 1984;Saifi and Chandra 1999;Skuse 2005;Dean and Mank 2014;Payseur et al 2018). Past work has suggested that the X chromosome may exhibit different evolutionary dynamics from the autosomes due to its unique inheritance pattern and increased exposure to selection through male hemizygosity (Vicoso and Charlesworth 2006;Nam et al 2015;Charlesworth et al 2018;Muralidhar and Veller 2022;Harris and Garud 2023). Recently, we found evidence in a North American D. melanogaster population that the X chromosome experiences an enrichment of hard selective sweeps compared to autosomes due to the increased visibility of new deleterious mutations to natural selection on the hemizygous X of males and reduced effective population size on the X (Harris and Garud 2023).…”

“…Past work has suggested that the X chromosome may exhibit different evolutionary dynamics from the autosomes due to its unique inheritance pattern and increased exposure to selection through male hemizygosity (Vicoso and Charlesworth 2006;Nam et al 2015;Charlesworth et al 2018;Muralidhar and Veller 2022;Harris and Garud 2023). Recently, we found evidence in a North American D. melanogaster population that the X chromosome experiences an enrichment of hard selective sweeps compared to autosomes due to the increased visibility of new deleterious mutations to natural selection on the hemizygous X of males and reduced effective population size on the X (Harris and Garud 2023). However, it is unclear whether this pattern of enrichment of hard sweeps on the X is a universal feature across all heterogametic species.…”

“…Recently, we found evidence of an enrichment of hard sweeps on the X chromosome compared to autosomes in a North American population of D. melanogaster (Harris and Garud 2023), suggesting that the X chromosome is subject to different evolutionary dynamics than the autosomes. Whether enrichment of hard sweeps on the X is a universal feature of molecular evolution has yet to be determined, as only a few species have been shown to have a higher prevalence of hard sweeps on the X compared to the autosomes (Nam et al 2015;Harris and Garud 2023). Quantifying the prevalence of hard versus soft sweeps in natural populations has been of great interest and debate (Peter et al 2012;Assaf et al 2015;Schrider et al 2015;Schrider and Kern 2016;Harris et al 2018b;Feder et al 2021;Garud et al 2021).…”

“…By leveraging whole genome samples from multiple species and populations (Arbiza et al 2014;Nam et al 2015;McGrath 2022), we can identify trends that are the norm across species, as well as exceptions that are indicative of the unique biology of individual species. However, four of the populations we analyze in this study have small sample sizes (n=7-23 samples), making it difficult to conduct the same haplotype-based scan Harris and Garud 2023) used in our previous work (Harris and Garud 2023). Additionally, each of these species has a unique demographic history for which we do not have accurate models, rendering our previous simulation-based approach for classifying putative sweeps as hard and soft challenging (Harris and Garud 2023).…”

Rapid evolutionary change, constraints and the maintenance of polymorphism in natural populations of Drosophila melanogaster

“…Indeed, many studies utilizing genome‐wide scans of selection have recovered signatures of well‐documented selection at genes such as Cyp6g1 , Ace and CHKov1 (e.g. see Duneau et al, 2018; Garud et al, 2021; Harris & Garud, 2023; Kapun et al, 2020). Single‐gene studies are also important in their own right, as they can help us to better understand the myriad of mechanisms through which selection can act as well as the molecular functions and environmental conditions that drive it.…”