Comparative analysis reveals the complex role of histoblast nest size in the evolution of novel insect abdominal appendages in Sepsidae (Diptera)

Authors: Melicher, Dacotah; SU, KATHY - National University Of Singapore; MEIER, RUDOLF - National University Of Singapore; BOWSHER, JULIA - North Dakota State University

Submitted to: BMC Evolutionary Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/26/2018
Publication Date: 10/10/2018
Publication URL: http://handle.nal.usda.gov/10113/6471007
Citation: Melicher, D.M., Su, K., Meier, R., Bowsher, J.H. 2018. Comparative analysis reveals the complex role of histoblast nest size in the evolution of novel insect abdominal appendages in Sepsidae (Diptera). BMC Evolutionary Biology. 18:151. https://doi.org/10.1186/s12862-018-1265-3.
DOI: https://doi.org/10.1186/s12862-018-1265-3

Interpretive Summary: Biologists have long understood how evolution makes small changes to animals so they better fit the environment but very little research has been done on how animals evolve completely new or “novel” structures. This is because evolution usually works by modifying existing body parts rather than creating new ones. For instance, bird and bat wings are modified from the bones that form hands and fingers in other species. In contrast, the evolution of a new set of wings only occurs in mythology: the wings of a dragon, which has a set of wings sprouting from their back in addition to four limbs, would be a result of this type of evolution. Although less spectacular than dragon wings, examples of novelty in evolution do exist in nature. In this paper researchers from the USDA-ARS facility in Fargo, ND, North Dakota State University, and the National University of Singapore compare members from a family of closely related flies where some male flies have brush or wing-like appendages sprouting from their abdomens. This is a novelty because no other group of flies grows similar brushes, the cells that form the brushes normally grow into a skin-like sheet, and they are very different from those that produce legs and wings. These brushes are used by males during courtship and mating to attract females and traits involved in mating are known to evolve quickly. We chose a group of species with brushes of different sizes and complexity and some closely related species which do not grow them. We looked closely at the cells in young flies and compared across species to see if they are all growing the brushes the same way. We found several patterns of growth that show brushes grow differently in many species. This shows that newly evolved body parts can appear suddenly and change quickly even in closely related species. All traits were new at one point in time and then diversified creating impressive variety in nature. Many of these, such as flowers and fruit, had humble evolutionary beginnings that are now of global importance. By understanding how animals evolve novel traits we can better understand where the diversity we see in nature comes from and this can guide and inform our decisions in research in other species.

Technical Abstract: The abdominal appendages of flies in the family Sepsidae are sexually dimorphic, jointed, highly mobile, and used by males during courtship and mating. Abdominal appendages have a complex evolutionary history of gain and loss. The appendages develop from histoblast nests, and an increase in the number of histoblast cells is associated with the development of abdominal appendages in males of some species. Our goal was to test whether the developmental mechanism is the same across species by correlating histoblast nest cell number, nest size, and organism size with the presence and absence of the appendage in multiple species. We used fluorescent confocal microscopy to measure the histoblast nest area, cell number, cell size, and segment length for males and females of 17 species across 10 genera in the family Sepsidae. These species represent the evolutionary history of putative gains and losses of the abdominal appendages including one species that is part of a sister clade that lacks abdominal appendages and is ancestral to the primary gain of the appendage. Histoblast nest morphology of males in species that have larger appendages have enlarged nests sizes peaking in the 4th segment which is the segment that produces the abdominal appendages, and lesser enlargement in neighboring segments. Species with small appendages and sternite modification show little or no significant sexually dimorphic histoblast nest morphology. Additionally, females of one appendage-bearing species also have enlarged 4th segment histoblast nests representing a loss of sexual dimorphism. This indicates that sepsid abdominal appendages and modified sternites may be the product of different developmental mechanisms or that these mechanisms have been subject to selection pressure and modified over evolutionary time in this sexually selected trait.