Slow rate of molecular evolution in high-elevation hummingbirds

Abstract

Estimates of relative rates of molecular evolution from a DNA-hybridization phylogeny for 26 hummingbird species provide evidence for a negative association between elevation and rate of single-copy genome evolution. This effect of elevation on rate remains significant even after taking into account a significant negative association between body mass and molecular rate. Population-level processes do not appear to account for these patterns because (i) all hummingbirds breed within their first year and (ii) the more extensive subdivision and speciation of bird populations living at high elevations predicts a positive association between elevation and rate. The negative association between body mass and molecular rate in other organisms has been attributed to higher mutation rates in forms with higher oxidative metabolism. As ambient oxygen tensions and temperature decrease with elevation, the slow rate of molecular evolution in high-elevation hummingbirds also may have a metabolic basis. A slower rate of single-copy DNA change at higher elevations suggests that the dynamics of molecular evolution cannot be separated from the environmental context.

Figure 1

Consensus unweighted least-squares FITCH topology obtained (8) from a complete matrix of symmetrized ΔT_mH-C values rooted with the outgroup swift Chaetura pelagica; names refer to principal nonhermit lineages and relevant subfamilies and families of the Apodiformes (hummingbirds and swifts), and letter codes to species as plotted in Fig. 2. The ΔT_mH-C index was obtained through several steps that minimize inaccuracies in distance measures (8). First, the T₅₀H index was obtained by correcting raw median melting temperatures (T_m) for normalized percentage hybridization (NPH) through application of the second-order polynomial found to fit observed values of T₅₀H regressed on T_m so as to avoid the excessive experimental error inherent in raw measures of NPH. The resulting T₅₀H values were multiplied by the empirically determined scaling factor of 1.2 for percentage sequence divergence (27) and then corrected for homoplasy (28). Finally, these distances were converted to so-called delta (Δ) values by standardizing the melting temperatures of different-species (heterologous) hybrids to the melting temperatures of same-species (homologous) hybrids (8). After symmetrization (29), average path lengths (12) for the resulting ΔT_mH-C values were estimated from 1,000 unweighted least-squares FITCH topologies (30) generated for a corresponding number of bootstrap pseudoreplicate matrices drawn from the complete matrix of 2,025 reciprocal genetic distances (three, rarely fewer, replicates per comparison). Internode support as indicated by bootstrap percentages (out of 1,000, if <100%) suggests strong support for the symmetrized topology, which was stable to multiple-deletion jackknifing (12). [Reproduced with permission from ref. . (Copyright 1997, Society for Molecular Biology and Evolution).]

Figure 2

Scatter plot of average path lengths to ingroup hummingbirds [Fig. 1; measured from outgroup swift (Chaetura pelagica)] versus midpoint of elevational occurrence. Taxa coded by principal lineage (symbol) and species (letter codes as indicated in Fig. 1). Overlapping symbols moved to reveal letter codes. Dashed lines indicate the 95% confidence intervals for least-squares regression of nonhermits. Folded F tests indicate significantly less variation in fitted path lengths measured from swift compared with those measured from either hermit [F′ = 9.93 (Threnetes), F′ = 11.48 (Eutoxeres); df = 23, 23; P < 0.0001], consistent with autocorrelation and saturation effects for the more distant swift comparison. The two hermits give virtually identical results except that distances are uniformly shortened when the more slowly evolving Eutoxeres aquila is used as the reference taxon for relative-rate estimates.