Flight loss linked to faster molecular evolution in insects

Abstract

The loss of flight ability has occurred thousands of times independently during insect evolution. Flight loss may be linked to higher molecular evolutionary rates because of reductions in effective population sizes (Ne) and relaxed selective constraints. Reduced dispersal ability increases population subdivision, may decrease geographical range size and increases (sub)population extinction risk, thus leading to an expected reduction in Ne. Additionally, flight loss in birds has been linked to higher molecular rates of energy-related genes, probably owing to relaxed selective constraints on energy metabolism. We tested for an association between insect flight loss and molecular rates through comparative analysis in 49 phylogenetically independent transitions spanning multiple taxa, including moths, flies, beetles, mayflies, stick insects, stoneflies, scorpionflies and caddisflies, using available nuclear and mitochondrial protein-coding DNA sequences. We estimated the rate of molecular evolution of flightless (FL) and related flight-capable lineages by ratios of non-synonymous-to-synonymous substitutions (dN/dS) and overall substitution rates (OSRs). Across multiple instances of flight loss, we show a significant pattern of higher dN/dS ratios and OSRs in FL lineages in mitochondrial but not nuclear genes. These patterns may be explained by relaxed selective constraints in FL ectotherms relating to energy metabolism, possibly in combination with reduced Ne.

Keywords: comparative method; effective population size; flight loss; mitochondrial genes; molecular evolutionary rates; selective constraints.

Figure 1.

(a) Summary of dN/dS ratio results for whole trees and (b) OSR results for whole trees between FL and F insects in eight studies. Each study (represented by grouped bars) includes phylogenies each containing multiple transitions to flightlessness (42 separate instances of flight loss total). Each result bar represents a gene or genes. The y-axis represents the dN/dS ratio or OSR of the FL lineages minus the dN/dS ratio or OSR of the F lineages; therefore, a positive bar height indicates that the FL lineages have higher dN/dS ratios or longer branch lengths than the F lineages with which it was compared. Bar labels are in the form ‘study’–‘gene’ ‘no. independent cases of flight loss for that gene’ ‘(no. of species in tree used)’. For example, W-EF1a 7(55) is study ‘W’—gene ‘EF1a’, ‘seven’ cases of loss (‘55’ species). Studies: W[19], Sn[20], M[21], S[22], C[23], P[24], Wi[5], Wh[26]. Phasm., Phasmatodea; Mec., Mecoptera. (Online version in colour.)

Figure 2.

Comparison of dN/dS ratios in FL and F lineages. (a) Thirty sister-clade comparisons involving mitochondrial genes and (b) 26 sister-clade comparisons involving nuclear genes. Each bar represents an individual instance of flight loss. A positive bar height indicates a sister comparison in which the dN/dS ratio is higher in the FL group than in the F group. Bar labels indicate the (‘study and reference number for the transition’) and the genes. Studies: W[19], Sn[20], M[21], S[22], C[23], P[24], Wi[5], Wh[26], D[25], Po[27], H[28], Pe[29], Mi[30], Z[31], Mu[33]. Transition reference numbers correspond to clade labels shown in the electronic supplementary material, figures S1–S8. (Online version in colour.)