Support for Y-compensation of mother’s curse affecting lifespan in Drosophila melanogaster
Abstract
Mother’s curse refers to male-biased deleterious mutations that may accumulate on the mitochondria due to its strict maternal inheritance. If these mutations persist, males should ideally compensate through mutations on the Y-chromosome given its strict paternal inheritance. Previous work has addressed this hypothesis by comparing coevolved and non-coevolved Y-mitochondria pairs placed alongside foreign autosomal backgrounds, expecting males with coevolved pairs to exhibit greater fitness due to Y-compensation. To date, no evidence of Y-compensation has been found. Such an experimental design assumes that Y-chromosomes compensate via direct interaction with mitochondria and/or is independent of autosome evolutionary history. If Y-chromosomes instead compensate by modifying autosomal targets, then this design could obscure Y-compensation by disrupting Y-autosome or mitochondria-autosome coadaptation. Here we address whether Y-chromosomes could ameliorate mitochondrial mutations affecting male lifespan in Drosophila melanogaster. Using three disparate populations we compared lifespan among males with coevolved and non-coevolved Y-mitochondria pairs placed alongside autosomal backgrounds coevolved with mitochondria. We found coevolved pairs exhibited a lower mortality risk relative to non-coevolved pairs. No such pattern was observed when coevolved and non-coevolved pairs were placed alongside non-coevolved autosomes, as with previous studies. These data are consistent with Y-compensation and highlight the importance of autosomes in this capacity. We cannot however exclude the possibility that Y-autosomal coevolution independent of mitochondrial mutations contributed to our results. Regardless, modern practices in medicine, conservation, and agriculture that introduce foreign Y-chromosomes into non-coevolved genetic backgrounds should be used with caution, as they may disrupt Y-autosome coadaptation and/or inadvertently unbridle mother’s curse.
README: Y-compensation
https://doi.org/10.5061/dryad.59zw3r2ht
Data are longevity values for 27 drosophila melanogaster genotypes that vary in the origin of their Y-chromosome, autosomes, and mitochondria. The genetic elements were derived from three stocks from the National Drosophila Species Stock Center (NDSSC) and include Montpellier, France; Cusco, Peru; and Cape Town, South Africa. All possible combinations of the genetic elements were created.
Description of the data and file structure
Data files consist of a master data file (titled "Longevity") that contains ALL of the data, and 17 other data files that partition the data into subsets to facilitate analysis in R. While the "Longevity" file contains all 5 genotypes, the "novel" file contains the YAM and yAM genotypes (represents our novel experimental design) and the "previous" file contains the YaM and yam genotypes (represents the previous works experimental design). Each of these files are further divided into the respective AM groups (AM=autosomal and mitochondrial). Thus, "novelSSSFSS" contains the YAM and yAM genotypes SSS and FSS respectively. The R script used for the analysis is also included (filename: "R script for anlaysis").
Data headers include ID, Vial, Y, A, M, AMgroup, Geno, TRT, and Long. Header descriptors are as follows:
ID: individual id number
Vial: unique number that identifies plastic vial in which flies were housed during the experiment
Y: Y-chromosome origin (F=France, P = Peru, S = South Africa)
A: Autosome origin
M: Mitochondrial origin
AMgroup: combination of the autosome and mitochondrial origin
Geno: individual's full genotype as the combination of the Y, A, and M genetic elements
TRT: treatment. Five treatments exist based on the combination of the genetic elements and include YAM (all elements coevolved. listed as CoEvo in datasheet), YaM (Y and mito coevolved, autosomes foreign. Listed as Y*M in datasheet), yAM (autosomes and mito coevolved, Y foreign. listed as *AM in datasheet), YAm (Y and autosomes coevolved, mito foreign. listed as YA_ in datasheet), and yam (all elements non-coevolved. Listed as Non in datasheet). The different treatment names in the datasheet was used because some analysis programs are not cap sensitive.
Long: longevity of individual in days.
Sharing/Access information
n/a
Code/Software
code for analysis provided as Word document in the data.zip folder