Fly wing vein patterns have spatial reproducibility of a single cell

Abstract

Developmental processes in multicellular organisms occur in fluctuating environments and are prone to noise, yet they produce complex patterns with astonishing reproducibility. We measure the left-right and inter-individual precision of bilaterally symmetric fly wings across the natural range of genetic and environmental conditions and find that wing vein patterns are specified with identical spatial precision and are reproducible to within a single-cell width. The early fly embryo operates at a similar degree of reproducibility, suggesting that the overall spatial precision of morphogenesis in Drosophila performs at the single-cell level. Could development be operating at the physical limit of what a biological system can achieve?

Keywords: Drosophila; development; fly wings; pattern formation; precision; symmetry.

Figure 1.

Wing vein patterns are naturally precise. (a) Right wing of a male Drosophila adult fly. The coordinates of seven wing vein crossings (landmarks) quantify principal pattern features. Green crosses indicate landmark positions of the depicted wing, respectively in all panels. Close-up of the two most proximal landmarks (black rectangle) with the Procrustes superimposed landmark distribution from right wings of (b) 41 flies raised under optimal conditions (OreR raised at 18°C) and (c) 22 flies from a natural population (caught in Cartagena, Colombia, raised at 22°C). Individual landmark locations are shown for females and males in red and blue, respectively. Green scale bar represents linear dimension of an average wing cell. Individual cells are marked by a bristle in the centre and cell size is measured from the distances between bristles. (b) Corresponds to the distribution where we observed the smallest landmark dispersion and (c) to the largest one. (d) Various systematic measurement errors (Σ_err) on the location of landmark locations (electronic supplementary material). Horizontal green line is the average spread of landmark distributions (〈Σ 〉 = 6.5 ± 0.7 µm) across male wings of all fly lines (N = 143), see text. (Online version in colour.)

Figure 2.

LR and inter-individual patterning precision range between 0.5 and 1 cell diameter for various genetic and environmental conditions. LR precision for fly populations of different genetic makeup (a) and at different growth temperatures (b) is measured as the spatial within-individual landmark variation , and shown as a function of the average linear wing cell size of the population. Females are indicated by black circles. In (a), all flies are raised in a controlled environment at 22°C; in (b), identical genetic background (OreR) is used. In both cases, the LR precision of the vein pattern is unaffected and remains at half a cell size (dotted lines have a slopes of 0.5 and 1.0). (c,d) LR versus inter-individual precision under varying genetic (c) and temperature (d) conditions. LR precision (y-axis) and inter-individual (x-axis) precision are measured in units of the linear wing cell size. Flies are on average more symmetric than reproducible (dashed line with a slope of 1 for identity). However, under controlled genetic and environmental conditions (in the most inbred fly lines in (c) and at 18°C in (d)) the left and right wing of a fly are as similar to each other, as they are to the wings of other flies of the same line. Thus, inter-individual and LR patterning precision are equal. Inbreds raised at 28°C (black data in (d)) show no reduction in inter-individual precision. Inset in (d) shows the net difference in the location of landmark 2 between two inbred populations raised at 22°C (light green data in (c)) and at 28°C (black data in (d)), exemplifying that flies with the same genetic makeup raised at two different temperature set-points can have distinct average landmark configurations (green and black crosses indicating error bars), which remain within a single cell and with a single cell and with an LR precision of half a cell diameter. (Online version in colour.)