Altitudinal clinal variation in wing size and shape in African Drosophila melanogaster: one cline or many?

Abstract

Geographical patterns of morphological variation have been useful in addressing hypotheses about environmental adaptation. In particular, latitudinal clines in phenotypes have been studied in a number of Drosophila species. Some environmental conditions along latitudinal clines-for example, temperature-also vary along altitudinal clines, but these have been studied infrequently and it remains unclear whether these environmental factors are similar enough for convergence or parallel evolution. Most clinal studies in Drosophila have dealt exclusively with univariate phenotypes, allowing for the detection of clinal relationships, but not for estimating the directions of covariation between them. We measured variation in wing shape and size in D. melanogaster derived from populations at varying altitudes and latitudes across sub-Saharan Africa. Geometric morphometrics allows us to compare shape changes associated with latitude and altitude, and manipulating rearing temperature allows us to quantify the extent to which thermal plasticity recapitulates clinal effects. Comparing effect vectors demonstrates that altitude, latitude, and temperature are only partly associated, and that the altitudinal shape effect may differ between Eastern and Western Africa. Our results suggest that selection responsible for these phenotypic clines may be more complex than just thermal adaptation.

Figure 1

(a) Map of approximate locations of the populations from which our lines are derived. (b) A representative wing image, with fitted B-splines. The colour-coded circles are the locations of the control points used to adjust the spline fit. (c) & (d) represent the spread of variation in our sample. (c) shows the grand mean shape, with circles indicating the positions of the landmarks and semi-landmarks extracted from the splines. The background blur is composed of the 112 within-line mean shapes from experiment 1. (d) shows the within-sex grand mean shapes, over a background blur composed of the 3008 individual wing shapes from experiment 1.

Figure 2

The influence of altitude on wing morphology. (a) Wing shape, represented as model-adjusted shape score, plotted against altitude. Each point is the within-sex mean for a single line. The altitude-shape relationship is similar in males and females. The black line shows the altitude-shape relationship modelled with the sexes pooled, with the grey region indicating 95 random draws from the posterior distribution. (b) The relationship between altitude and wing size; points are within-sex line means, and the grey regions indicate 95 random draws from the posterior distribution. Altitude is associated with an increase in wing size in both sexes. (c) Visualisation of the variation represented by the model-adjusted shape score, scaled to 3x the difference between lowest and highest populations. Most of the changes seem to be localized to medial and proximal regions of the wings, including shifting of the crossveins and an expansion of the posterior lobe at high altitudes.

Figure 3

The joint influence of thermal plasticity and altitude of origin on wing morphology (a) The altitude-shape relationship for both sexes and rearing temperatures. Points are within-sex line means. At 24°C the relationship is similar between males and females. This pattern changes at 18°C, with the altitude-shape relationship maintained in females but weakened in males. (b) The altitude-wing size relationship for both sexes at both rearing temperatures. Points are within-sex line means. Both sexes’ wings are larger at 18°C, but whereas the slope of the altitude-size relationship is consistent between temperatures in males, females show a steeper relationship at 18°C than at 24°C. (c) Visualizations of the altitude-shape effect, calculated separately within each rearing temperature. Between them is their vector correlation (95% credible interval).

Figure 4

Vector correlations between model-adjusted effects on shape. Points are vector correlations between posterior mean coefficient vectors for pairs of modelled effects, with lines representing 95% credible intervals on the vector correlations. Coefficients are calculated simultaneously from the full model for each experiment. While most vector correlations indicate weak to moderate relationships between these effects, notably rearing temperature and allometric scaling effects appear very similar, as well as rearing temperature and latitude of origin.

Figure 5

Altitudinal co-variation with shape differs between populations from Eastern and Western Africa. As demonstrated with both the shape scores and vector correlations between altitudinal effects from Eastern and Western African populations, there appears to be largely distinct influences on shape. (a) Altitude and wing shape, represented as model-adjusted shape score calculated separately for western and eastern population groups (see Figure 1). Each point is the within-sex mean for a single line. (b) Altitude and wing shape, represented as model-adjusted shape score calculated separately for Cameroonian and Ethiopian populations. Each point is an individual. (c) Visualizations of the shape effects associated with altitude calculated separately as labelled. Between pairs of effects are their vector correlations (95% credible intervals)