Abstract
The capacity of regenerating a new structure after losing an old one is a major challenge in the animal kingdom. Fish have emerged as an interesting model to study regeneration due to their high and diverse regenerative capacity. To date, most efforts have focused on revealing the mechanisms underlying fin regeneration, but information on why and how this capacity evolves remains incomplete. Here, we propose the livebearing fish family Poeciliidae as a promising new model system to study the evolution of fin regeneration. First, we review the current state of knowledge on the evolution of regeneration in the animal kingdom, with a special emphasis on fish fins. Second, we summarize recent advances in our understanding of the mechanisms behind fin regeneration in fish. Third, we discuss potential evolutionary pressures that may modulate the regenerative capacity of fish fins and propose three new theories for how natural and sexual selection can lead to the evolution of fin regeneration: (1) signaling-driven fin regeneration, (2) predation-driven fin regeneration, and (3) matrotrophy-suppressed fin regeneration. Finally, we argue that fish from the family Poeciliidae are an excellent model system to test these theories, because they comprise of a large variety of species in a well-defined phylogenetic framework that inhabit very different environments and display remarkable variation in reproductive traits, allowing for comparative studies of fin regeneration among closely related species, among populations within species or among individuals within populations. This new model system has the potential to shed new light on the underlying genetic and molecular mechanisms driving the evolution and diversification of regeneration in vertebrates.
Highlights
Regeneration is one of the most intriguing phenomena in nature
M2 macrophages remained high in number while the M1 macrophage population decreased in the wound area, suggesting that M2 macrophages are likely involved in the remodeling of cells during fin regeneration (Nguyen-Chi et al, 2017)
This idea is further supported by recent studies on adult zebrafish showing that macrophages are capable of attenuating inflammation after injuries (Hasegawa et al, 2017) and that macrophage accumulation within the regenerating tissue is needed for proper fin regeneration, in line with a pro-regenerative gene profile (Sanz-Morejón et al, 2019)
Summary
Regeneration is one of the most intriguing phenomena in nature. In the last decades, the capacity of regenerating a damaged or lost structure has been a central interest for scientists. The cellular mechanisms that underlie the regeneration program can be remarkably diverse, suggesting that perhaps regeneration is not an ancestral trait but that instead it represents a novel innovation that has evolved independently many times in different phyla as an adaptive trait (Tiozzo and Copley, 2015) It is not clear yet how regeneration evolves, three potential causes have been proposed to explain a lack of, or reduced, regenerative ability in animals (Bely, 2010): (1) The first is that the regenerative capacity becomes restricted as the individual keeps developing, due to a reduction of cellular plasticity. In particular, are increasingly recognized as a relevant model to understand the factors shaping regenerative capacity, because next to their primary function (i.e., swimming) (i), fins are often fundamental for secondary functions that directly impact fitness (e.g., swimming, feeding, reproduction) and (ii) are (contrary to other regenerative tissues, such as the heart and spinal cord) often directly exposed to biotic and abiotic factors
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