Genetic Architecture of Two Fitness-related Traits in Drosophila melanogaster: Ovariole Number and Thorax Length

Abstract

In Drosophila melanogaster, ovariole number and thorax length are morphological characters thought to be associated with fitness. Maximum daily egg production in females is positively correlated with ovariole number, while thorax length is correlated with male reproductive success and female fecundity. Though both traits are related to fitness, ovariole number is likely to be under stabilizing selection, while thorax length appears to be under directional selection. Current research has focused on examining the sources of variation for ovariole number in relation to fitness, with a view towards elucidating how segregating variation is maintained in natural populations. Here, we utilize a diallel design to explore the genetic architecture of ovariole number and thorax length in nine isogenic lines derived from a natural population. The full diallel design allows the estimation of general combining ability (GCA), specific combining ability (SCA), and also describes variation due to reciprocal effects (RGCA and RSCA). Ovariole number and thorax length differed with respect to their genetic architecture, reflective of the independent selective forces acting on the traits. For ovariole number, GCA accounted for the majority (67.3%) of variation segregating between the lines, with no evidence of reciprocal effects or inbreeding depression; SCA accounted for a small percentage (3.9%) of the variance, suggesting dominance variation; no reciprocal effects were observed. In contrast, for thorax length, the majority of the non-error variance was accounted for by SCA (17.9%), with only one third as much variance (6.2%) due to GCA. Interestingly, RSCA (nuclear-extranuclear interactions) accounted for slightly more variation (7.5%) than GCA in these data. Thus, genetic variation for thorax length is largely in accord with predictions for a fitness trait under directional selection: little additive genetic variation and substantial dominance variation (including a suggestion of inbreeding depression); while the mechanisms underlying the maintenance of variation for ovariole number are more complex.

Quantitative Trait Loci Affecting Phenotypic Plasticity and the Allometric Relationship of Ovariole Number and Thorax Length in Drosophila melanogaster

“…The correlations within environments, between traits, decreased monotonically with increasing yeast level (Table 5, Figure 2) and were significantly different from zero in all environments (nominal P , 2e À16 , P ¼ 2.5e À5 , P ¼ 0.0013, and P ¼ 0.0089 for 0.2, 0.4, 0.6, and 0.8% yeast by volume, respectively). A significant genetic correlation between ovariole number and thorax length within populations has not been previously reported (Wayne et al 1997;Telonis-Scott et al 2005), where measurements were made on flies reared under high yeast concentrations. QTL analysis: QTL analysis for ovariole number and thorax length identified the same QTL within any given environment and when phenotypes were concatenated across environments with environment used as an additive covariate.…”

“…While there is considerable information about the molecular and quantitative genetic basis for adult body size (e.g., Wayne et al 1997Wayne et al , 2001Leevers and Hafen 2003;Oldham and Hafen 2003;Hafen 2004;Caldwell et al 2005;Colombani et al 2005;Mirth et al 2005) and ovariole number (Coyne et al 1991;Wayne et al 1997Wayne et al , 2001Hodin and Riddiford 1998;Wayne and Mackay 1998;Wayne and McIntyre 2002;Telonis-Scott et al 2005;Orgogozo et al 2006) in D. melanogaster and related species, little is known about the genetic basis for nutrient-induced phenotypic plasticity in these traits.…”

Effects of larval crowding on quantitative variation for development time and viability in Drosophila melanogaster

“…Although natural selection is expected to erode such variation, several studies have shown that there is abundant genetic variation for fitness‐related traits in natural populations (Fanara, Folguera, Iriarte, Mensch, & Hasson, 2006; Ledón‐Rettig, Pfennig, & Crespi, 2010; McGuigan, Nishimura, Currey, Hurwit, & Cresko, 2010; Paaby et al., 2015; Telonis‐Scott, McIntyre, & Wayne, 2005). This puzzling fact has been explained various ways (e.g., Barton & Turelli, 1989).…”

Convergent evolution of a reproductive trait through distinct developmental mechanisms in Drosophila

“…Albeit not to single-gene resolution, these investigations have shown that ovariole number is a polygenic trait (Coyne et al, 1991;Thomas-Orillard, 1976), and inter-and intraspecific ovariole number variation is linked to changes at numerous loci (Bergland et al, 2008;Orgogozo et al, 2006;Telonis-Scott et al, 2005;Wayne et al, 2001;Wayne and McIntyre, 2002). Determining promising candidate genes from these QTL studies is difficult, because ovarian morphogenesis is relatively poorly understood, and only a small number of genes have been shown to play a specific role in ovariole formation (Gancz et al, 2011;Godt and Laski, 1995;Hodin and Riddiford, 1998).…”