Genome size variation affects song attractiveness in grasshoppers: Evidence for sexual selection against large genomes

Abstract

Genome size is largely uncorrelated to organismal complexity and adaptive scenarios. Genetic drift as well as intragenomic conflict have been put forward to explain this observation. We here study the impact of genome size on sexual attractiveness in the bow-winged grasshopper Chorthippus biguttulus. Grasshoppers show particularly large variation in genome size due to the high prevalence of supernumerary chromosomes that are considered (mildly) selfish, as evidenced by non-Mendelian inheritance and fitness costs if present in high numbers. We ranked male grasshoppers by song characteristics that are known to affect female preferences in this species and scored genome sizes of attractive and unattractive individuals from the extremes of this distribution.We find that attractive singers have significantly smaller genomes, demonstrating that genome size is reflected in male courtship songs and that females prefer songs of males with small genomes. Such a genome size dependent mate preference effectively selects against selfish genetic elements that tend to increase genome size. The data therefore provide a novel example of how sexual selection can reinforce natural selection and can act as an agent in an intragenomic arms race. Furthermore, our findings indicate an underappreciated route of how choosy females could gain indirect benefits.

Genome size correlates with reproductive fitness in seed beetles

“…Although Huang et al [27] failed to find significant covariation between GS and phenotypic traits, Ellis et al [28] documented significant but environment-dependent covariation between GS and several life-history traits across a subset of these inbred lines. Schielzeth et al [29] revealed a negative association between male song attractiveness and GS in the grasshopper Chorthippus biguttulus, suggesting that sexual selection may act to reduce GS. In this species, however, variation in the number of supernumerary chromosomes (rather than more common sources of variation in GS) likely caused, or at least contributed to, the observed pattern.…”

Comment on Schielzeth et al. (2014): “Genome size variation affects song attractiveness in grasshoppers: Evidence for sexual selection against large genomes”

“…() but not by Schielzeth et al. (). This omission is important since López‐León et al.’s results are not consistent with Schielzeth et al.’s conclusion that B chromosomes are involved in sexual selection against large genomes, especially considering that the analysis of mating pairs in the field is very likely relevant to actual fitness compared to analyses of mating or courtship song in the laboratory.…”

“…Schielzeth et al. () measured DNA content by two techniques, namely flow cytometry and a photometric approach using a Nanodrop 2000 instrument, on nuclei obtained from the isolated heads of 24 attractive and 24 unattractive males. Flow cytometry is a very accurate technique to estimate DNA content when coefficients of variation are lower than 8% (Shankey et al.…”

Technical Comment: Response to Camacho

“…We had recently reported an association between song attractiveness and genome size in a population of bow‐winged grasshoppers, Chorthippus biguttulus , with unattractive singers having larger genomes (Schielzeth et al. ). Camacho () commented on our publication expressing doubts whether the data support our conclusions.…”