Abstract
SynopsisFree-swimming planktonic larvae are a key stage in the development of many marine phyla, and studies of these organisms have contributed to our understanding of major genetic and evolutionary processes. Although transitory, these larvae often attain a remarkable degree of tissue complexity, with well-defined musculature and nervous systems. Among the best studied are larvae belonging to the phylum Echinodermata, but with work largely focused on the pluteus larvae of sea urchins (class Echinoidea). The greatest diversity of larval strategies among echinoderms is found in the class Asteroidea (sea stars), organisms that are rapidly emerging as experimental systems for genetic and developmental studies. However, the bipinnaria larvae of sea stars have only been studied in detail in a small number of species and although they have been relatively well described neuro-anatomically, they are poorly understood neurochemically. Here, we have analyzed embryonic development and bipinnaria larval anatomy in the common North Atlantic sea star Asterias rubens, using a variety of staining methods in combination with confocal microscopy. Importantly, the chemical complexity of the nervous system of bipinnaria larvae was revealed through use of a diverse set of antibodies, with identification of at least three centers of differing neurochemical signature within the previously described nervous system: the anterior apical organ, oral region, and ciliary bands. Furthermore, the anatomy of the musculature and sites of cell division in bipinnaria larvae was analyzed. Comparisons of developmental progression and molecular anatomy across the Echinodermata provided a basis for hypotheses on the shared evolutionary and developmental processes that have shaped this group of animals. We conclude that bipinnaria larvae appear to be remarkably conserved across ∼200 million years of evolutionary time and may represent a strong evolutionary and/or developmental constraint on species utilizing this larval strategy.
Highlights
Species from many marine phyla develop via a biphasic lifestyle, transitioning from a free-swimming planktonic larva to a more sedentary benthonic adult
Patiria miniata and A. rubens have nearly identical bipinnaria larvae despite representing different asteroid super-orders that diverged 200 million years ago (Lafay et al 1995; Linchangco et al 2017)
The feeding bipinnaria is present by 3 dpf in P. miniata and P. pectinifera (Murabe et al 2021) but not until 5–6 dpf in Pisaster ochraceus and A. rubens (Pia et al 2012)
Summary
Species from many marine phyla develop via a biphasic lifestyle, transitioning from a free-swimming planktonic larva to a more sedentary benthonic adult. Echinoderm larvae are typically characterized based upon how nutrition is obtained before metamorphosis: either free-feeding planktotrophs with complex ciliary bands, or lecithotrophs dependent on a maternally derived yolky substance (Zamora et al 2020) Within these categories, there is considerable diversity and some species display highly derived developmental progressions that do not fall neatly within these two sub-divisions (McEdward 1995; Byrne et al 2007). It belongs to the order Forcipulatida and is distantly related to the valvatids P. miniata and P. pectinifera, but closely related to another forcupilatid—Pisaster ochraeus (Mah and Foltz 2011) These species are the asteroids in which the larval nervous system has previously been characterized in detail, and studies on A. rubens allow for comparisons across both deep and shallow phylogenetic distances. This work enables comparisons of the development of the nervous system and other structures across the planktonic larvae of the Echinodermata to better provide an understanding of the evolutionary and developmental processes that have shaped the biodiversity of the group
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