Mitochondrial polymorphism shapes intrapopulation behavioural variation in wild Drosophila

Abstract

Intrapopulation variation in behaviour, including activity, boldness and aggressiveness, is becoming more widely recognized and is hypothesized to substantially affect ecological and evolutionary dynamics. Although previous studies used candidate-gene approaches and genome-wide association analyses to identify genes correlated with variations in activity and aggressiveness, behavioural variation may not be fully captured in the nuclear genome, as it does not account for mitochondrial genomes. Mitochondrial genes encode products that are key regulators of the cellular energy-producing pathways in metabolic processes and are thought to play a significant role in life-history and reproductive traits. In this study, we considered many isofemale lines of Drosophila immigrans established from two wild populations to investigate whether intrapopulation variation in the mitochondrial genome affected activity level within this species. We identified two major haplogroups in these populations, and activity levels in both larvae and adults differed significantly between the two haplogroups. This result indicated that intrapopulation variation in activity level may be partially controlled by mitochondrial genes, along with the interaction between nuclear and mitochondrial genes and the age of individual organisms.

Ecology, the pace‐of‐life, epistatic selection and the maintenance of genetic variation in life‐history genes

“…However, recent research has associated mtDNA polymorphism with key rate-dependent LH and related phenotypes, such as development time (Christie et al, 2004;Erić et al, 2022), longevity (Jelić et al, 2015), stress resistance (Jelić et al, 2015;Sun et al, 2019), general activity (Ueno & Takahashi, 2021) and even metabolic rate (Baris et al, 2017;Đorđević et al, 2016;Kurbalija Novičić et al, 2015). Second, observations such as those of stable mtDNA haplotype frequencies over time and space (Andrianov et al, 2008;Oliver et al, 2005) MacRae & Anderson, 1988;Oliver et al, 2005).…”

“…First, within‐population mtDNA polymorphism is very common, but was long assumed to be non‐functional and neutral. However, recent research has associated mtDNA polymorphism with key rate‐dependent LH and related phenotypes, such as development time (Christie et al, 2004; Erić et al, 2022), longevity (Jelić et al, 2015), stress resistance (Jelić et al, 2015; Sun et al, 2019), general activity (Ueno & Takahashi, 2021) and even metabolic rate (Baris et al, 2017; Đorđević et al, 2016; Kurbalija Novičić et al, 2015). Second, observations such as those of stable mtDNA haplotype frequencies over time and space (Andrianov et al, 2008; Oliver et al, 2005), environmental clines in haplotype frequencies (McKenzie et al, 2019; Silva et al, 2014) and widespread polymorphism of deeply divergent mtDNA haplotype families (Kvie et al, 2013) are all consistent with balancing selection.…”

“…This inclusive definition expands upon a narrower population genetic definition, where the fitness of a genotype is density independent and defined only by its frequency, to include more realistic and complex scenarios where NFDS emerges from density-dependent selection (Antonovics & Kareiva, 1988;Clarke, 1979;Kisdi, 1999;Mallet, 2012;Wallace, 1975). We note that theory predicts that this form of NFDS can favour the evolution of a genetic architecture which is 'concentrated' to one or a few regions, corresponding to polymorphisms in traits that are related to ecological competition (Kopp & Hermisson, 2006;Schneider, 2007;van Doorn & Dieckman, 2005;Yeaman, 2022).…”