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Evolutionary parallelisms of pectoral and pelvic network-anatomy from fins to limbs.

ABSTRACT: Lobe-fins transformed into limbs during the Devonian period, facilitating the water-to-land transition in tetrapods. We traced the evolution of well-articulated skeletons across the fins-to-limbs transition, using a network-based approach to quantify and compare topological features of fins and limbs. We show that the topological arrangement of bones in pectoral and pelvic appendages evolved in parallel during the fins-to-limbs transition, occupying overlapping regions of the morphospace, following a directional trend, and decreasing their disparity over time. We identify the presence of digits as the morphological novelty triggering topological changes that discriminated limbs from fins. The origin of digits caused an evolutionary shift toward appendages that were less densely and heterogeneously connected, but more assortative and modular. Disparity likewise decreased for both appendages, more markedly until a time concomitant with the earliest-known tetrapod tracks. Last, we rejected the presence of a pectoral-pelvic similarity bottleneck at the origin of tetrapods.

SUBMITTER: Esteve-Altava B

PROVIDER: S-EPMC6506248 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Evolutionary parallelisms of pectoral and pelvic network-anatomy from fins to limbs.

Esteve-Altava Borja B Pierce Stephanie E SE Molnar Julia L JL Johnston Peter P Diogo Rui R Hutchinson John R JR

Science advances 20190508 5

Lobe-fins transformed into limbs during the Devonian period, facilitating the water-to-land transition in tetrapods. We traced the evolution of well-articulated skeletons across the fins-to-limbs transition, using a network-based approach to quantify and compare topological features of fins and limbs. We show that the topological arrangement of bones in pectoral and pelvic appendages evolved in parallel during the fins-to-limbs transition, occupying overlapping regions of the morphospace, follow ...[more]

PMID: 31086814

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Project description:Fins of fishes provide many examples of structures that are beautifully designed to power and control movement in water; however, some species also use their fins for substrate-associated behaviors where interactions with solid surfaces are key. Here, we examine how the pectoral fins of ray-finned fish with these multifunctional behavioral demands, in water and on solid surfaces, are structured and function. We subdivide fins used in swimming and substrate contact into two general morphological categories, regionalized vs. generalized fins. Regionalized fins have ventral rays that are free from connecting membrane or in which that membrane is reduced. Dorsally they maintain a more typical membranous fin. While all pectoral fins vary somewhat in their morphology from leading to trailing edge, generalized fins do not have the substantial membrane loss between rays that is seen in regionalized fins and the distal edge anatomy changes gradually along its margin. We add a new case study in regionalized fins with the dwarf hawkfish (Cirrhitichthys falco). Hawkfishes are most often found perching and moving on structures in their environments. During perching, the free ventral rays are in contact with the substrate and splayed. We found that unlike other fish with regionalized pectoral fins, hawkfish maintain use of the dorsal membranous region of its pectoral fin for rhythmic swimming. We found that typically hawkfish bend their ventral free rays under, toward the medial hemitrichs or hold them straight during substrate-associated postures. This appears also to be the case for the ventral free rays of other species with regionalized fins. Generalized fin use for substrate contact was reviewed in round gobies (Neogobius melanostomus). In addition, although their lobe fins are not representative of ray-finned fish anatomy, we explored fin contact on submerged substrates in the Senegal bichir (Polypterus senegalus), which has a generalized distal fin (no free fin rays or distinct membrane regions). Both groups use their pectoral fins for swimming. During substrate-based postures, unlike hawkfish, their distal rays generally bend outward toward the lateral hemitrichs and a large swath of the fin membrane can contact the surface. The alternative demands on multifunctional fins suggest specialization of the mechanosensory system. We review mechanosensation related to fin movement and surface contact. These alternative regionalized and generalized strategies for serving aquatic and substrate-based functions underwater provide opportunities to further investigate specializations, including sensory structures and systems, that accompany the evolution of substrate-based behaviors in vertebrates.

Dataset Information

Evolutionary parallelisms of pectoral and pelvic network-anatomy from fins to limbs.

Publications

Evolutionary parallelisms of pectoral and pelvic network-anatomy from fins to limbs.

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