Evolutionary crossroads in developmental biology: Cyclostomes (lamprey and hagfish)

Department of Zoology, University of Oxford, The Tinbergen Building, South Parks Road, Oxford OX1 3PS, UK.
Development (Impact Factor: 6.46). 06/2012; 139(12):2091-9. DOI: 10.1242/dev.074716
Source: PubMed


Lampreys and hagfish, which together are known as the cyclostomes or 'agnathans', are the only surviving lineages of jawless fish. They diverged early in vertebrate evolution, before the origin of the hinged jaws that are characteristic of gnathostome (jawed) vertebrates and before the evolution of paired appendages. However, they do share numerous characteristics with jawed vertebrates. Studies of cyclostome development can thus help us to understand when, and how, key aspects of the vertebrate body evolved. Here, we summarise the development of cyclostomes, highlighting the key species studied and experimental methods available. We then discuss how studies of cyclostomes have provided important insight into the evolution of fins, jaws, skeleton and neural crest.

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Available from: Sebastian M Shimeld, Oct 16, 2015
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    • "A second outstanding controversy to which the concept of tetralogy may apply concerns the uncertainty surrounding the relative timing of the vertebrate 1R/2R WGD events to the divergence of agnathans and gnathostomes (Kuraku 2008; Shimeld and Donoghue 2012). Extant agnathans, comprising hagfish and lampreys, have many duplicated genes in similar proportions to gnathostomes, but when phylogenetic trees are constructed clear 1:1 orthologies with gnathostome genes are often absent (Escriva et al. 2002; Irvine et al. 2002; Stadler et al. 2004; Qiu et al. 2011; Fujimoto et al. 2013). "
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    ABSTRACT: Numerous ancient whole genome duplications (WGD) have occurred during eukaryote evolution. In vertebrates, duplicated developmental genes and their functional divergence have had important consequences for morphological evolution. While two vertebrate WGD events (1R/2R) occurred over 525 Myr ago, we have focussed on the more recent 3R or TGD (teleost genome duplication) event which occurred ~350 Myr ago in a common ancestor of over 26,000 species of teleost fishes. Through a combination of whole genome and BAC clone sequencing we characterized all Hox gene clusters of Pantodon buchholzi, a member of the early branching teleost subdivision Osteoglossomorpha. We find 45 Hox genes organized in only five clusters indicating that Pantodon has suffered more Hox cluster loss than other known species. Despite strong evidence for homology of the five Pantodon clusters to the four canonical pre-TGD vertebrate clusters (one HoxA, two HoxB, one HoxC and one HoxD), we were unable to confidently resolve 1:1 orthology relationships between four of the Pantodon clusters and the eight post-TGD clusters of other teleosts. Phylogenetic analysis revealed that many Pantodon genes segregate outside the conventional 'a' and 'b' post-TGD orthology groups, that extensive topological incongruence exists between genes physically linked on a single cluster, and that signal divergence causes ambivalence in assigning 1:1 orthology in concatenated Hox cluster analyses. Out of several possible explanations for this phenomenon we favour a model which keeps with the prevailing view of a single TGD prior to teleost radiation, but which also considers the timing of diploidization after duplication, relative to speciation events. We suggest that while the duplicated hoxa clusters diploidized prior to divergence of osteoglossomorphs, the duplicated hoxb, hoxc, and hoxd clusters concluded diploidization independently in osteoglossomorphs and other teleosts. We use the term 'tetralogy' to describe the homology relationship which exists between duplicated sequences which originate via a shared WGD, but which diploidize into distinct paralogs from a common allelic pool independently in two lineages following speciation.
    Molecular Biology and Evolution 06/2014; 31(10). DOI:10.1093/molbev/msu202 · 9.11 Impact Factor
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    • "Lampreys and hagfish are jawless fish whose ancestors diverged from the other vertebrates more than 500 million years ago [1], [2]. Modern lampreys have retained many features of early vertebrates, although they also exhibit lineage-specific morphologic and molecular traits [3], [4]. Consequently, these animals serve as model system for the study of complex features, such as vascular blood coagulation or the endothelium-lined, pressurized circulatory system that emerged at the rise of vertebrates [5]. "
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    ABSTRACT: Vertebrates evolved an endothelium-lined hemostatic system and a pump-driven pressurized circulation with a finely-balanced coagulation cascade and elaborate blood pressure control over the past 500 million years. Genome analyses have identified principal components of the ancestral coagulation system, however, how this complex trait was originally regulated is largely unknown. Likewise, little is known about the roots of blood pressure control in vertebrates. Here we studied three members of the serpin superfamily that interfere with procoagulant activity and blood pressure of lampreys, a group of basal vertebrates. Angiotensinogen from these jawless fish was found to fulfill a dual role by operating as a highly selective thrombin inhibitor that is activated by heparin-related glycosaminoglycans, and concurrently by serving as source of effector peptides that activate type 1 angiotensin receptors. Lampreys, uniquely among vertebrates, thus use angiotensinogen for interference with both coagulation and osmo- and pressure regulation. Heparin cofactor II from lampreys, in contrast to its paralogue angiotensinogen, is preferentially activated by dermatan sulfate, suggesting that these two serpins affect different facets of thrombin's multiple roles. Lampreys also express a lineage-specific serpin with anti-factor Xa activity, which demonstrates that another important procoagulant enzyme is under inhibitory control. Comparative genomics suggests that orthologues of these three serpins were key components of the ancestral hemostatic system. It appears that, early in vertebrate evolution, coagulation and osmo- and pressure regulation crosstalked through antiproteolytically active angiotensinogen, a feature that was lost during vertebrate radiation, though in gnathostomes interplay between these traits is effective.
    PLoS ONE 05/2014; 9(5):e97879. DOI:10.1371/journal.pone.0097879 · 3.23 Impact Factor
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    • "Since not all genes fit within this rule it is assumed that gene deletion or amplification has taken place in order to fit the 2R hypothesis. It has been considered that the divergence between agnathans and gnathostomes occurred at some time before the 2R-WGD [19]–[21], however, recent studies suggest that at least the sea lamprey genome has also suffered this second whole genome duplication event [22]–[24]. "
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    ABSTRACT: Recently there has been much interest in the Regulators of Calcineurin (RCAN) proteins which are important endogenous modulators of the calcineurin-NFATc signalling pathway. They have been shown to have a crucial role in cellular programmes such as the immune response, muscle fibre remodelling and memory, but also in pathological processes such as cardiac hypertrophy and neurodegenerative diseases. In vertebrates, the RCAN family form a functional subfamily of three members RCAN1, RCAN2 and RCAN3 whereas only one RCAN is present in the rest of Eukarya. In addition, RCAN genes have been shown to collocate with RUNX and CLIC genes in ACD clusters (ACD21, ACD6 and ACD1). How the RCAN genes and their clustering in ACDs evolved is still unknown. After analysing RCAN gene family evolution using bioinformatic tools, we propose that the three RCAN vertebrate genes within the ACD clusters, which evolved from single copy genes present in invertebrates and lower eukaryotes, are the result of two rounds of whole genome duplication, followed by a segmental duplication. This evolutionary scenario involves the loss or gain of some RCAN genes during evolution. In addition, we have analysed RCAN gene structure and identified the existence of several characteristic features that can be involved in RCAN evolution and gene expression regulation. These included: several transposable elements, CpG islands in the 5' region of the genes, the existence of antisense transcripts (NAT) associated with the three human genes, and considerable evidence for bidirectional promoters that regulate RCAN gene expression. Furthermore, we show that the CpG island associated with the RCAN3 gene promoter is unmethylated and transcriptionally active. All these results provide timely new insights into the molecular mechanisms underlying RCAN function and a more in depth knowledge of this gene family whose members are obvious candidates for the development of future therapies.
    PLoS ONE 01/2014; 9(1):e85539. DOI:10.1371/journal.pone.0085539 · 3.23 Impact Factor
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