Making quantitative morphological variation from basic developmental processes: Where are we? The case of the Drosophila wing

Abstract

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.

Modularity: Genes, Development, and Evolution

“…This model was successful at producing accurate predictions of tooth morphology for several mammalian groups (Salazar-Ciudad & Jernvall 2010). Other successful cases of the use of developmental mechanisms to explain phenotypic variation comes from Drosophila wing venation patterns (Matamoro-Vidal et al 2015) and butterfly wing spots (Beldade & Brakefield 2002), both of which involve changes in several key developmental processes, such as the distribution of morphogens in the wing disc or the establishment of planar cell polarity.…”

Drosophilawing modularity revisited through a quantitative genetic approach

“…; Mackay 2010; Matamoro‐Vidal et al. ), is a proper model to study the evolution and development of quantitative morphological variation. The modular organization of this complex morphological structure has been repeatedly assessed to understand the mechanisms that generate covariation and predict the response of wing shape to natural selection (Klingenberg and Zaklan ; Klingenberg ).…”

“…), which is also known as proximal wing (Whitworth and Russell ) or wing hinge (Matamoro‐Vidal et al. ). The wing blade is defined as the area that corresponds to the distal domain of expression of the gene vestigial ( vg ), whereas the wing base roughly corresponds to the domain of expression of the zinc finger homeodomain ( zfh2 ) gene (Terriente et al.…”

“…Later in pupal development, the wing disc folds and extends in the evagination process and the wing is elongated along the PD axis (Matamoro‐Vidal et al. ). At 15 hours after pupation the wing is evenly divided into the proximal hinge and the distal blade.…”

Lack of interruption of the gene network underlying wing polyphenism in an early‐branching ant genus

“…To determine whether the wing GRN in the wing discs of winged queen castes in Mystrium is conserved relative to Drosophila and the winged castes of derived species, we first compared the shape of their wing discs. The wing disc of Drosophila is a relatively flat structure with a circular area that will eventually fold into a bilayered pouch to form the wing, and a proximal elongated area that will develop into the wing hinge and the body wall (Matamoro‐Vidal, Salazar‐Ciudad, & Houle, ). Despite these minor differences in shape between Mystrium and Drosophila , homologous regions of the discs are easily identified.…”