SummaryHow tissues acquire their characteristic shape is a fundamental unresolved question in biology. While genes have been characterized that control local mechanical forces to elongate epithelial tissues, genes controlling global forces in epithelia have yet to be identified. Here, we describe a genetic pathway that shapes appendages in Drosophila by defining the pattern of global tensile forces in the tissue. In the appendages, shape arises from tension generated by cell constriction and localized anchorage of the epithelium to the cuticle via the apical extracellular-matrix protein Dumpy (Dp). Altering Dp expression in the developing wing results in predictable changes in wing shape that can be simulated by a computational model that incorporates only tissue contraction and localized anchorage. Three other wing shape genes, narrow, tapered, and lanceolate, encode components of a pathway that modulates Dp distribution in the wing to refine the global force pattern and thus wing shape.
One of the aims of evolutionary developmental biology is to discover the developmental origins of morphological variation. The discipline has mainly focused on qualitative morphological differences (e.g., presence or absence of a structure) between species. Studies addressing subtle, quantitative variation are less common. The Drosophila wing is a model for the study of development and evolution, making it suitable to investigate the developmental mechanisms underlying the subtle quantitative morphological variation observed in nature. Previous reviews have focused on the processes involved in wing differentiation, patterning and growth. Here, we investigate what is known about how the wing achieves its final shape, and what variation in development is capable of generating the variation in wing shape observed in nature. Three major developmental stages need to be considered: larval development, pupariation, and pupal development. The major cellular processes involved in the determination of tissue size and shape are cell proliferation, cell death, oriented cell division and oriented cell intercalation. We review how variation in temporal and spatial distribution of growth and transcription factors affects these cellular mechanisms, which in turn affects wing shape. We then discuss which aspects of the wing morphological variation are predictable on the basis of these mechanisms.
Cell competition is a widespread process leading to the expansion of one cell population through the elimination and replacement of another. A large number of genetic alterations can lead to either competitive elimination of the mutated population or expansion of the mutated cells through the elimination of the neighbouring cells. Several processes have been proposed to participate in the preferential elimination of one cell population, including competition for limiting extracellular pro-survival factors, communication through direct cell-cell contact, or differential sensitivity to mechanical stress. Recent quantitative studies of cell competition have also demonstrated the strong impact of the shape of the interfaces between the two populations. Here, we discuss the direct and indirect contribution of mechanical cues to cell competition, where they act either as modulators of competitive interactions or as direct drivers of cell elimination. We first discuss how mechanics can regulate contact-dependent and diffusion-based competition by modulating the shape of the interface between the two populations. We then describe the direct contribution of mechanical stress to cell elimination and competition for space. Finally, we discuss how mechanical feedback also influences compensatory growth and triggers preferential expansion of one population.
The wall of pollen grains exhibits morphological variation in many features including apertures, ornamentation and thickness, but the function of these characters remains to be clarified. It has been suggested that they are involved in the accommodation of volume changes (harmomegathy). To investigate this further, we developed a protocol that induces a controlled hydration of the pollen without affecting its metabolism and we applied it to six species differing in their pollen wall morphology. The entry of water caused pollen swelling and volume increase leading to breakage of the wall and/or of the plasma membrane, such that the per cent of intact grains was negatively correlated with the level of hydration. Qualitative and quantitative differences were observed between the species. Breakage of the exine was observed only in pollen lacking apertures and with thin exine. Variation in the exine ornamentation and thickness could explain the interspecific differences observed for the rates of breakage of the plasma membrane. Our results suggest that pollen wall morphology matters for survival and maintenance of pollen integrity further to volume increase due to hydration. We propose a rationale for future studies that should allow disentangling the contribution of different pollen morphological and physiological features to harmomegathy.
Aperture patterns, i.e., number, shape, and position, influence the capacity to accommodate volume variations in pollen grains. When subjected to water inflow, pollen grains with few apertures survive better than pollen with many apertures. Trade-offs between survival and germination are likely to be involved in the evolution of pollen morphology.
Although much attention has been paid to the role of stabilizing selection, empirical analyses testing the role of developmental constraints in evolutionary stasis remain rare, particularly for plants. This topic is studied here with a focus on the evolution of a pollen ontogenetic feature, the last points of callose deposition (LPCD) pattern, involved in the determination of an adaptive morphological pollen character (aperture pattern). The LPCD pattern exhibits a low level of evolution in eudicots, as compared to the evolution observed in monocots. Stasis in this pattern might be explained by developmental constraints expressed during male meiosis (microsporogenesis) or by selective pressures expressed through the adaptive role of the aperture pattern. Here, we demonstrate that the LPCD pattern is conserved in Euphorbiaceae s.s. and that this conservatism is primarily due to selective pressures. A phylogenetic association was found between the putative removal of selective pressures on pollen morphology after the origin of inaperturate pollen, and the appearance of variation in microsporogenesis and in the resulting LPCD pattern, suggesting that stasis was due to these selective pressures. However, even in a neutral context, variation in microsporogenesis was biased. This should therefore favour the appearance of some developmental and morphological phenotypes rather than others.
Summary The contribution of developmental constraints and selective forces to the determination of evolutionary patterns is an important and unsolved question. We test whether the long‐term evolutionary stasis observed for pollen morphogenesis (microsporogenesis) in eudicots is due to developmental constraints or to selection on a morphological trait shaped by microsporogenesis: the equatorial aperture pattern. Most eudicots have three equatorial apertures but several taxa have independently lost the equatorial pattern and have microsporogenesis decoupled from aperture pattern determination. If selection on the equatorial pattern limits variation, we expect to see increased variation in microsporogenesis in the nonequatorial clades. Variation of microsporogenesis was studied using phylogenetic comparative analyses in 83 species dispersed throughout eudicots including species with and without equatorial apertures. The species that have lost the equatorial pattern have highly variable microsporogenesis at the intra‐individual and inter‐specific levels regardless of their pollen morphology, whereas microsporogenesis remains stable in species with the equatorial pattern. The observed burst of variation upon loss of equatorial apertures shows that there are no strong developmental constraints precluding variation in microsporogenesis, and that the stasis is likely to be due principally to selective pressure acting on pollen morphogenesis because of its implication in the determination of the equatorial aperture pattern.
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