Inferring developmental modularity from morphological integration: Analysis of individual variation and asymmetry in bumblebee wings

Organisms are built from distinct modules, which are internally coherent bu t flexible in their relationships among one another. We examined morphologi cal variation within and between two candidate modules: the fore- and hindw ings of bumblebees (Hymenoptera: Apidae: Bombus empatiens). We used the tec hniques of geometric morphometrics (Procrustes superimposition) to analyze the variation of landmark configurations in fore- and hindwings. Regression was used to correct for size-related shape variation (allometry). Principa l component analysis revealed patterns of variation that were remarkably si milar for individual variation and fluctuating asymmetry (FA). Because cova riation of FA among parts must be due to direct transmission of the develop mental perturbations causing FA, this agreement of patterns suggests that m uch of individual variation is also due to direct developmental interaction s within each developing wing. Moreover, partial least squares analysis ind icated that the patterns of shape covariation between fore- and hindwings w ere nearly the same as the patterns of within-wing variation. Shape covaria tion of FA was only found in bees that had been reared under elevated CO2 c oncentration but not in bees from the control treatment, suggesting that th e mechanisms of developmental interactions between fore- and hindwings are related to gas exchange. We conclude that the fore- and hindwings are devel opmental modules that maintain internal coherence through direct developmen tal interactions and are connected to each other only by relatively few lin ks that use the system of interactions within modules.