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Proc Biol Sci
2022 May 11;2891974:20220258. doi: 10.1098/rspb.2022.0258.
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Heterochrony and parallel evolution of echinoderm, hemichordate and cephalochordate internal bars.
Álvarez-Armada N
,
Cameron CB
,
Bauer JE
,
Rahman IA
.
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Deuterostomes comprise three phyla with radically different body plans. Phylogenetic bracketing of the living deuterostome clades suggests the latest common ancestor of echinoderms, hemichordates and chordates was a bilaterally symmetrical worm with pharyngeal openings, with these characters lost in echinoderms. Early fossil echinoderms with pharyngeal openings have been described, but their interpretation is highly controversial. Here, we critically evaluate the evidence for pharyngeal structures (gill bars) in the extinct stylophoran echinoderms Lagynocystis pyramidalis and Jaekelocarpus oklahomensis using virtual models based on high-resolution X-ray tomography scans of three-dimensionally preserved fossil specimens. Multivariate analyses of the size, spacing and arrangement of the internal bars in these fossils indicate they are substantially more similar to gill bars in modern enteropneust hemichordates and cephalochordates than to other internal bar-like structures in fossil blastozoan echinoderms. The close similarity between the internal bars of the stylophorans L. pyramidalis and J. oklahomensis and the gill bars of extant chordates and hemichordates is strong evidence for their homology. Differences between these internal bars and bar-like elements of the respiratory systems in blastozoans suggest these structures might have arisen through parallel evolution across deuterostomes, perhaps underpinned by a common developmental genetic mechanism.
Figure 1. . Virtual reconstructions of internal bars and bar-like structures in modern and fossil deuterostomes. (a) Lagynocystis pyramidalis (NHMUK E29043), external view showing the position of the internal bars. (b) Close-up of the internal bars in Lagynocystis pyramidalis (NHMUK E16107, left; NHMUK E29453, right). (c) Generalized diagram visualizing the distribution and morphological characteristics of the internal bars in Lagynocystis pyramidalis. (d) Cryptoschisma sp. (MGM-3383D), external view (left) and close-up of a single hydrospire group (right). (e) Generalized diagram visualizing the distribution and morphological characteristics of the hydrospires folds (bar-like structures) in Hyperoblastus reimanni and Crysptoschisma sp.; however, the latter lacks slits in the C-D interray. (f) Strobilocystites polleyi (CMC IP 36209), external view showing the position of the rhomb-pores (top) and close-up of a single rhomb-pore bearing complex (bottom). (g) Generalized diagram visualizing the distribution and morphological characteristics of the pores (bar-like structures) in Strobilocystites polleyi. (h) Schizocardium sp., lateral views showing external and internal morphological features. (i) Branchiostoma floridae, lateral views showing external and internal morphological features. (j) Generalized diagram visualizing the distribution and morphological characteristics of the gill bars in hemichordates and cephalochordates. Scale bars = 1 mm.
Figure 2. . Linear discriminant analysis (LDA) (a,c) and principal component analysis (PCA) (b,d) of the dimensions (length, width, depth and spacing) of internal bars and bar-like structures in modern and fossil deuterostomes. (a) LDA plot of the resultant morphospace. (b) PCA plot of the resultant morphospace. (c,d) Biplot vectors showing the contribution of each dimension of the internal bars and bar-like structures to the variation in the dataset for LDA (c) and PCA with vectors colour coded by the square cosines contribution to the variation of the data (d). Abbreviations: B.f, Branchiostoma floridae; B.sp, Balanoglossus sp.; C.sp, Cryptoschisma sp.; H.r, Hyperoblastus reimanni; J.o, Jaekelocarpus oklahomensis; L.p1, Lagynocystis pyramidalis (NHMUK E29453); L.p2, Lagynocystis pyramidalis (NHMUK E16107); S.p, Strobilocystites polleyi.; S.sp, Schizocardium sp. (Online version in colour.)
Figure 3. . A generalized phylogenetic tree of the deuterostomes showing the evolution of key characters linked to the pharyngeal openings.
Brauner,
Ontogeny and paleophysiology of the gill: new insights from larval and air-breathing fish.
2012, Pubmed
Brauner,
Ontogeny and paleophysiology of the gill: new insights from larval and air-breathing fish.
2012,
Pubmed
Cameron,
Evolution of the chordate body plan: new insights from phylogenetic analyses of deuterostome phyla.
2000,
Pubmed
Cameron,
Particle retention and flow in the pharynx of the enteropneust worm Harrimania planktophilus: the filter-feeding pharynx may have evolved before the chordates.
2002,
Pubmed
Caron,
Tubicolous enteropneusts from the Cambrian period.
2013,
Pubmed
,
Echinobase
Clausen,
Palaeoanatomy and biological affinities of a Cambrian deuterostome (Stylophora).
2005,
Pubmed
Cole,
The nature and significance of invertebrate cartilages revisited: distribution and histology of cartilage and cartilage-like tissues within the Metazoa.
2004,
Pubmed
Dominguez,
Paired gill slits in a fossil with a calcite skeleton.
2002,
Pubmed
,
Echinobase
Ezhova,
The nephridial hypothesis of the gill slit origin.
2015,
Pubmed
Fritzenwanker,
The Fox/Forkhead transcription factor family of the hemichordate Saccoglossus kowalevskii.
2014,
Pubmed
,
Echinobase
Gillis,
A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network.
2012,
Pubmed
Glenn Northcutt,
The new head hypothesis revisited.
2005,
Pubmed
Han,
Meiofaunal deuterostomes from the basal Cambrian of Shaanxi (China).
2017,
Pubmed
Kapli,
Lack of support for Deuterostomia prompts reinterpretation of the first Bilateria.
2021,
Pubmed
Larouche-Bilodeau,
Filter feeding, deviations from bilateral symmetry, developmental noise, and heterochrony of hemichordate and cephalochordate gills.
2020,
Pubmed
,
Echinobase
Nanglu,
Cambrian suspension-feeding tubicolous hemichordates.
2016,
Pubmed
Ogasawara,
Developmental expression of Pax1/9 genes in urochordate and hemichordate gills: insight into function and evolution of the pharyngeal epithelium.
1999,
Pubmed
Okai,
Characterization of gill-specific genes of the acorn worm Ptychodera flava.
2000,
Pubmed
Ou,
Evidence for gill slits and a pharynx in Cambrian vetulicolians: implications for the early evolution of deuterostomes.
2012,
Pubmed
,
Echinobase
Rombough,
The functional ontogeny of the teleost gill: which comes first, gas or ion exchange?
2007,
Pubmed
Rychel,
Development and evolution of chordate cartilage.
2007,
Pubmed
Simakov,
Hemichordate genomes and deuterostome origins.
2015,
Pubmed
,
Echinobase
Swalla,
Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives.
2008,
Pubmed
,
Echinobase
Witten,
Bone without minerals and its secondary mineralization in Atlantic salmon (Salmo salar): the recovery from phosphorus deficiency.
2019,
Pubmed
Wright,
The unusual cartilaginous tissues of jawless craniates, cephalochordates and invertebrates.
2001,
Pubmed
Yasui,
Development of oral and branchial muscles in lancelet larvae of Branchiostoma japonicum.
2014,
Pubmed
Zhang,
The sea cucumber genome provides insights into morphological evolution and visceral regeneration.
2017,
Pubmed
,
Echinobase
Álvarez-Armada,
Heterochrony and parallel evolution of echinoderm, hemichordate and cephalochordate internal bars.
2022,
Pubmed
,
Echinobase
