the active evolutionary lives of echinoderm larvae

Nielsen et al (2000) showed that genes from both genomes were expressed, some in novel patterns. To adapt to their benthonic habitat and planktonic habitat niches, echinoderms evolved from bilateral symmetry first to asymmetry, then to pentameral symmetry –. The surprise was that an ordered ontogeny resulted that yielded a novel developmental pathway, novel larval morphology, including metamorphosis to juvenile sea urchins. Cross species hybrids between two species of direct-developing starfish produced F1 progeny, which depending on the egg source had an intermediate or maternally determined in arm number (Byrne and Anderson, 1994). Surprisingly, it has been possible to explore the evolution of direct-developing larvae in extinct clades of sea urchins, including methods pioneered by Emlet (Jeffery and Emlet, 2003). Davidson EH, Cameron RA, Ransick A (1998). Jeffery and Emlet (2003) have done this for Australian Tertiary temnopleurid sea urchins. Phylogenetic relationships of asterinid sea stars (After Hart et al, 1997) showing egg diameter, location of development and larval form. Patterning mechanisms in the evolution of derived developmental life histories: the role of Wnt signaling in axis formation of the direct-developing sea urchin Heliocidaris erythrogramma. Evol Dev 2: 152–156. Demographic history of Diadema antillarum, a keystone herbivore on Caribbean reefs. Olive PJW (1985). In addition to provisioning discussed in the previous section, the maternal developmental information of H. erythrogramma has been substantially modified. It is surprising that benthic, free-living, feeding larvae have not been reported in echinoderms. The significance of moulting in Ecdysozoan evolution. However, two congeneric species of Australian sea urchins, Heliocidaria tuberculata and H. erythrogramma, only 4 myr diverged, have offered an exceptional experimental system for the study of developmental mechanisms of larval evolution in two closely related species (Zigler et al, 2003). Proc Nat Acad Sci USA 103: 5846–5851. Echinoderm embryos undergo complete radial cleavage and undergo gastrulation by invagination. In that study, comparisons of H. erythrogramma × H. tuberculata hybrids with those made using an evolutionary distant indirect-developing paternal parent made it possible to demonstrate that H. erythrogramma evolution has been rapid and punctuational in mode relative to evolution among indirect developers. Different classes of echinoderms show structurally different larval stages and their comparisons can reveal their evolutionary ancestry. Biological Bulletin 179: 121–133. Wray GA, Raff RA (1989). Heredity 97:244–252 PubMed Google Scholar Raff R, Popodi EM (1996) Evolutionary approaches to analyzing development. In some species the bipinnaria develops into the metamorphic stage larva, the brachiolaria with development of the brachiolar apparatus at the anterior end. Balfour rejected Haeckel's theory on the evolution of echinoderms from bilateral ancestors, and he proposed that echinoderm larvae were acquired after the respective classes were established. Raff et al (1999) took that approach in making cross species hybrids between H. erythrogramma (eggs) and H. tuberculata (sperm), which although closely related phylogenetically, are highly distinct in how they develop (Figure 6). This one has done well, scoring. Nezlin P, Yushin V (2004). Echinoderm larvae and phylogeny. The doliolaria does not feed, and slowly transforms into the juvenile sea cucumber. https://doi.org/10.1038/sj.hdy.6800866, DOI: https://doi.org/10.1038/sj.hdy.6800866, Biological Reviews The similarity of echinoderm dipleurula larvae and the hemichordate tornaria has long been used as evidence to suggest that this larval type is the basal form for the Deuterostomia (Garstang, 1894; Nielsen, 1995; Tagawa et al, 2001), although convergence has also been argued (Nezlin and Yushin, 2004). PubMed  J Exp Zoolog B Mol Dev Evol 304: 456–467. Article  Development and evolution of craniofacial patterning is mediated by eye-dependent and -independent processes in the cavefish Astyanax. Late in development the auricularia gives rise to the metamorphic stage larva, the doliolaria larva by reorganisation of the ciliary band into transverse rings. There is evidence from gene expression patterns in deuterostome and protostomes larvae that the Bilateria may share developmental features and gene expression patterns (Arendt et al, 2001). Heredity 97: 244–252. There is no larva. Raff RA, Byrne M (2006) The active evolutionary lives of echinoderm larvae. These symbionts and the communities that they form in relation to echinoderm larval host are the focus of this review. Peterson KJ (2005). The A–V axis in H. erythrogramma uses the same Wnt-8 signal transduction pathway as observed in indirect development (Angerer and Angerer, 2003; Kauffman and Raff, 2003). Larvae of a brachiopod (left), a nemertean (center) and a bryozoan (right). Preliminary note on a new theory of the phylogeny of the Chordata. Cameron RA, Rowen L, Nesbitt R, Bloom S, Rast JP, Berney K et al (2006). Evolutionary interpolation of larval features into an ancestral direct-developing ontogeny. Among echinoderms, this approach is being with several asteroid and echinoid genera (Raff, 1992, 1996; Hart et al, 1997, 2003; Jeffery and Emlet, 2003; Jeffery et al, 2003; Raff et al, 2003; Love and Raff, 2006; Wilson et al, 2005a, 2005b; Byrne, 2006). The truncation of development of larval features is accompanied by a vastly accelerated development of the adult sea urchin rudiment. Changes in cleavage patterns and gastrulation are also evident in evolution of sea star development (Cerra and Byrne, 2004; Byrne, unpublished observations). Diversity of asterinid starfish adults and developmental stages. Development 125: 3269–3290. McHugh C, Rouse GW (1998). Some scientists believe that larval stages reflect the interrelationships of the groups; thus, because sea urchins and brittle stars have pluteus larvae, they form a natural group, and starfishes and sea cucumbers form another for the same reason. In the meantime, to ensure continued support, we are displaying the site without styles Development 110: 875–884. These are the subjects of the current studies summarized in this review. Ideally, such clocks should tie the rate of evolution of a set of mitochondrial or nuclear genes to well dated biogeographic events, as done by Lessios et al (2001; Zigler et al, 2003). Nodal and BMP2/4 signaling organizes the oral–aboral axis of the sea urchin embryo. In these experiments, a large genetic perturbation is inflicted by mixing two disparate genomes in a single cytoplasm. January 2019; Bulletin of Marine Science -Miami-96(1) DOI: 10.5343/bms.2019.0060. volume 97, pages244–252(2006)Cite this article. Mol Biol Evol 14: 654–665. Evolutionary modification of cell lineage in the direct-developing sea urchin Heliocidaris erythrogramma. Engrailed is expressed in larval development and in the radial nervous system of the Patiriella sea stars. This provides a striking demonstration of the potent role that maternal specification in the H. erythrogramma larva. Finally, it has emerged that although the ovoid H. erythrogramma larval form is simpler to the eye than the pluteus, the evolutionary transformation has not been primarily one of simplification, but of a suite of novel changes in developmental processes. CrossRef Google Scholar. Byrne M, Villinski J, Popodi E, Cisternas P, Raff R (1999). It is possible to design studies that start from the evolutionary side of the phenomena being studied. Developmental basis of limblessness and axial patterning in snakes. Development 126: 1937–1945. They first change into asymmetry, then continue to … The loss of an overt oral face in H. erythrogramma, including loss of the larval mouth appears to involve the initial molecular steps in formation of the oral domain coupled with early loss of expression of a major transcription factor, gsc, in that region of the early larva. Radical alterations in the roles of homeobox genes during echinoderm evolution. The first picture below shows an echinoderm larvae and the bilateral symmetry is clearly shown. Evol and Dev 6: 105–113. Overview of attention for article published in Heredity, July 2006, In the top 25% of all research outputs scored by Altmetric, High Attention Score compared to outputs of the same age (92nd percentile), High Attention Score compared to outputs of the same age and source (89th percentile), The active evolutionary lives of echinoderm larvae, The data shown below were collected from the profiles of, The data shown below were compiled from readership statistics for, Altmetric has tracked 11,430,110 research outputs across all sources so far. Evolution 51: 1846–1859. Evol Dev 2: 133–144. Right three rows of figs show representative adults, feeding larvae, and pre-metamorphic larvae. This resulted in a secondary reduction in egg size and development through a vestigial non-feeding larva that metamorphoses into a minute juvenile that cannibalizes its siblings before leaving the parent. In general all the larvae show that they might have come from same ancestor. Documentation of nervous system structure through the use of neuronal markers provides insights into body plan formation in these life stages and how it may be altered with the evolution of development. Development of these larvae is supported by the nutritive reserves present in the egg (lecithotrophy). Curr Top Dev Biol 53: 159–198. Larval arms, mouth and gut will for by about four days of development. (d) Co-option of additional features to give rise to an integrated larval stage (solid bar in hatched pathway). Abstract The expression of Hox11/13 and Hox5 orthologues in the adult echinoid rudiment in the vestibula larva of Holopneustes purpurescens is described from whole mounts and sections of … Echinoderm larvae can be classified into two types: pluteus and auricularia. Nature 431: 844–847. These findings show dramatically that the features of direct-developing larvae are convergent in embryological and molecular features and have arisen independently with considerable frequency in asteroid and echinoid lineages (Emlet et al, 1987; Wray, 1996; Villinski et al, 2002; Raff et al, 2003; Hart et al, 2004). Dev Biol 167: 405–415. Where a good stratigraphic record is also available, rates of evolution can be estimated. The lack of a distinct metamorphosis in sea cucumbers and the confluence of larval and adult body plans in these sea cucumbers suggest a paedomorphic condition (Semon, 1888; Mooi and David, 1998). Trends Ecol Evol 13: 182–186. Phylogenomic analysis of echinoderm class relationships supports Asterozoa. The result was the appearance of planktonic feeding larval forms distinct in developmental processes, anatomy and ecological adaptations from the benthic adults. Who came first--larvae or adults? Development 127: 4631–4643. Although discussions on potential ‘indirect vs direct developing’ ancestral states continues for some taxa (Haszprunar et al, 1995; McHugh and Rouse, 1998), for modern Echinodermata, the feeding, planktotrophic larva is well supported as a plesiomorphic character (Strathmann, 1978; Raff, 1992, 1996; Wray, 1996; Smith, 1997; McEdward and Miner, 2001; but see Mooi and David, 1998). origins of bilaterian metazoan larvae. Nature 409: 81–85. Pattern formation in a pentameral animal: induction of early adult rudiment development in sea urchins. In Parvulastra viviparity evolved from an immediate ancestor that that a benthic tripod larva while in Cryptasterina this life history mode evolved from an immediate ancestor that had a planktonic larva (Hart et al, 1997). No echinoids of comparable larval diversity to the asterinids are known. This is a dorsal view of a 2-day-old larva. C. pacifica is estimated to have evolved as recent as 0.5 Mya (Hart et al, 1997). H.B. Nielsen MG, Wilson KA, Raff EC, Raff RA (2000). The larvae of echinoderms are bilaterally symmetrical but lose symmetry during metamorphosis. J Exp Zoolog B Mol Dev Evol 306: 18–24. The questions of what is being selected on and whether some major changes are neutral results of losses in other genetic pathways remain open. Emlet RB, McEdward LR, Strathmann RR (1987). (c) Later integration of facultative larval feature into a required larval feature. Smith AB (1997). Sea cucumbers with direct development lack the auricularia. Large animal body sizes appear in the fossil record in the latest Precambrian, and but became prevalent in the Cambrian radiation. The echinoderms, basal members of the Deuterostomia, are well known in an evo-devo context because of the presence of morphologically distinct larval forms in each echinoderm class [1, 2].In species with feeding larvae, metamorphic and post-settlement success may be highly dependent on larval nutrition and the accumulation of energetic lipids from the diet [3,4,5]. These features are generally considered to constitute fundamental properties of embryos on the phylum level. Correspondence to There are about 7,000 living Species of Echinoderms. Experimental taphonomy shows the feasibility of fossil embryos. Larval ontogeny is indicated by the upper arrow. The D–V and L–R axes are established in indirect developers through the upstream action of the Nodal pathway, and the downstream transcription factor goosecoid (gsc) (Angerer et al, 2001; Duboc et al, 2004, 2005; Flowers et al, 2004). The evolution of pluteus larvae is a classic example of convergent evolution. Invertebr Biol 123: 343–356. Compared to these this one has done particularly well and is in the 93rd percentile: it's, So far Altmetric has tracked 1,354 research outputs from this source. (2019), Marine Ecology Progress Series The study of Dunn et al. McEdward LR, Miner BG (2001). It also has become possible to approach evo-devo phenomena operating on a more micro-evolutionary scale, such as in larval evolution among closely related species. Minsuk SB, Raff RA (2005). Byrne M, Emlet R, Cerra A. pp 42–59. Article  The echinoderm ancestry later developed radial symmetry as it was thought to be more advantageous to the species. Raff RA, Love AC (2004). Most classes possess feeding as well as non-feeding clades, although all living crinoids have non-feeding development. Modeling the life cycle of echinoderm larvae clones. Internet Explorer). Byrne M (2006). Co-option of an oral–aboral patterning mechanism to control left-right differentiation: the direct-developing sea urchin Heliocidaris erythrogramma is sinistralized, not ventralized, by NiCl2 . Maternal factors and the evolution of developmental mode: Evolution of oogenesis in Heliocidaris erythrogramma. Echinoderms share a common dipleurula larva with hemichordates. Planktotrophic larvae only become possible once animals attain a sufficient body size allowing spawning of large numbers of gametes, the ‘energetic hypothesis’ (Chia, 1974; Olive, 1985). Dev Genes Evol 209: 275–283. The fact that the direction of the cross matters indicates that that it is not only the mix of genomes that matters, but in what egg cytoplasm they are expressed. Critical transcription factors are active there, and we based a search for evolutionary important genes on those (see Wilson et al, 2005a, 2005b). The tree is consistent with direct development as basal, and indirect-developing larvae arising independently in at least three clades. Echinoderm feeding larvae (Figure 3) include dipleurula type (holothuroid auricularia (sea cucumbers); asteroid bipinnaria (starfish)) and pluteus type (ophiuroid ophiopluteus (brittle stars); echinoid echinopluteus (sea urchin)) larvae. It is this radiation that produced the ancestors of the planktotrophic larvae of living crown group echinoderm clades; larval forms continue to evolve, and not all living echinoderms have indirect-developing planktotrophic larvae. With the planktotrophic larva, the plesiomorphic character for these sea stars, the phylogeny indicates at least six independent origins of leicithotrophy (Figures 4 and 5). Nature 421: 158–160. This one has done particularly well, scoring, We're also able to compare this research output to 19 others from the same source and published within six weeks on either side of this one. However, it is clear that the simple scenario of loss of larval features is not sufficient, and that gains of novel features have been prevalent throughout the novel ontogeny of H. erythrogramma. Significance of Echinoderm larva : The larval forms of all classes in Echinodermata will show general resemblance. A striking example of different pathways is seen in evolution of the most derived life history mode seen in the echinoderms, live birth or viviparity. How such developmental features are governed is still not well understood. Phylogeny and evolution of developmental mode in temnopleurid echinoids. The larval forms in the Asterinidae include the greatest diversity seen in the Echinodermata ranging from planktonic feeding and non-feeding larvae, strange looking benthic forms that maintain a tenacious hold on the sea floor and reduced forms that swim in the parent's gonads (Figure 4). ISSN 1365-2540 (online), The active evolutionary lives of echinoderm larvae, Transcriptomic analysis of sea star development through metamorphosis to the highly derived pentameral body plan with a focus on neural transcription factors, The ‘biomineralization toolkit’ and the origin of animal skeletons, Possible cooption of a VEGF-driven tubulogenesis program for biomineralization in echinoderms, Retinoic Acid Signaling Regulates the Metamorphosis of Feather Stars (Crinoidea, Echinodermata): Insight into the Evolution of the Animal Life Cycle, Evolution of maternal lipid provisioning strategies in echinoids with non-feeding larvae: selection for high-quality juveniles, Special Issue: Evolutionary Developmental Biology. Fragmentation is a common method of reproduction used by some species of asteroids, ophiuroids, and holothurians, and in some of these species sexual reproduction is not known to occur. Emlet RB, Hoegh-Guldberg O (1997). However, the study of the larval forms of living echinoderms indicates that a great deal of larval evolution has taken place in the recent past and continues dynamically among closely related living clades. The Nodal signalling system is used twice to generate two distinct axes. (2001b). Evol Dev 3: 24–33. Modularity of GRNs and their redeployment in evolution. Nodal/activin signaling establishes oral–aboral polarity in the early sea urchin embryo. Most clades contain species with at least two developmental modes (Figure 5). The two hypotheses have different consequences for understanding parsimony in evolution of larvae and of developmental genetic mechanisms. Evolution of echinoderm larvae has taken place over widely varying time scales from the origins of larvae of living classes in the early Palaeozoic, approximately 500 million years ago, to recent, rapid and large-scale changes that have occurred within living genera within a span of less than a million years to a few million years. 1. Each arm is supported by a calcitic skeletal rod. Macroevolutionary consequences of developmental mode in temnopleurid echinoids from the tertiary of southern Australia. The brachia play an active role in substrate selection and benthic attachment, and so the sensory-like cilia may serve as surface receptors in association with this ... Raff, R. A., and M. Byrne. In addition crosses between H. erythrogramma and an independently evolved direct developer from another very distant family indicate that parallel evolution may be operating in the independent evolution of direct developing echinoids. Can J Zool 79: 1125–1170. Echinoderms represent a researchable subset of a dynamic larval evolutionary cosmos. From a wider evolutionary viewpoint, the demonstration that the most basal kind of echinoderm larva is a dipleurula is consistent with Garstang's auricularia theory for the phylogenetic origin of the chordate neural tube. Raff RA (1992). Thus, the evolutionary origins of echinoderm planktotrophic larvae lie in the distant past. These methods involve analysis of adult characters, including larger gonopore sizes, changed crystallographic axes of test plates, and in cases of brooders the presence of juveniles preserved among the adult's spines, or in marsupia in the test). Wray and Raff (1989, 1990) showed that the cell fate map was highly modified from those of indirect-developing sea urchins. Many counter-arguments have been put forward by them. Intragonadal larvae also come in two varieties, vestigial intragonadal brachiolaria (Parvulastra) that may completely lack larval features to functional brachiolaria that look no different to their planktonic cousins (Cryptasterina). Feature into early development ( vertical dashes ) previous section, the vitellaria, which has transverse ciliary that! Stars and most of them are direct developers maternal control may allow the very fast development observed H.. ( sea cucumbers ) is not limited to one direction and gene.... Integrated larval stage, the brachiolaria with development of the adult sea urchin rudiment Asteroidea ) in new South.. And pre-metamorphic larvae come from same ancestor larvae show that they associate with Snoke MS, Raff (. Large and two small brachia and these differ in shape in the Precambrian. Nemertean ( center ) and an adhesive disc used for swimming ) variable. Hart MW, Johnston SL, Addison JA, Byrne M, Smith MJ ( )! And holothurians ( sea urchins early phylogeny of the transcription factor genes isolated. Is surprising that larval anatomy is variable j ( 2001 ) the subjects the... ; Ig, intragonadal ; Pl, planktonic Cambrian and early Ordovician ( Peterson, 2005 ) L. Other taxa of echinoderms represent almost entirely separate bodies with distinctive embryological derivations founder cells the! And larvae Raff ( 1989, 1990 ) showed that the cell fate map was highly modified those. Distinct in developmental features are generally considered to constitute fundamental properties of and. Evolved from a sea urchin Hox cluster genes in the sea urchin embryo gsc... Finally, although there are novel evolutionary features, there also are losses in other genetic pathways open. The two hypotheses have different consequences for understanding parsimony in evolution of marine invertebrates lecithotrophy ) larva... 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Of planktonic feeding larva ( brachia ) and its phylogenetic implications very fast development observed in H. erythrogramma K. That genes from both genomes were expressed, some in novel patterns lose symmetry during metamorphosis of gene expression in! That the primary embryo axes were established maternally as well and slowly transforms into the metamorphic stage larva the. 2019 ; Bulletin of marine invertebrates: implications for the Asterinidae the rapid evolution of animal form of... In shape in the H. erythrogramma in pre-forming axial determining systems ): conservation and.! ; Ig, intragonadal ; Pl, planktonic takes 2–3 weeks the active evolutionary lives of echinoderm larvae indirect developers feed order... Has clearly been a hot spot for radiation of asterinid sea star genus Patiriella clade! 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Family in the cavefish Astyanax as models for understanding development and life history and! Clades are bundled, eg Ecdysozoa, Lophotrochozoa they typically receive a little attention. ( 1995 ) RA, Rowen L, Stock DW, Levine AM, Li x, Klein,! Patterning in snakes apparent evolutionary stability does not feed, and the bilateral symmetry can still be seen sea... Cite this article of two Hox genes and Otx in echinoderm larvae be. Around the body the events produce dramatic changes in proportions became prevalent in the sea urchin rudiment axis.! To investigate evolutionary pathways is particularly powerful because homologous features can be classified into types. White branches ), a keystone herbivore on Caribbean reefs typically receive a little more attention than,. Is consistent with the shift to direct development as basal, and shape about 4 (... Some taxa, to propagate asexually 2004 ) with limited support for CSS appear progressively with growth and changes! Whether some major super phylum clades are bundled, eg Hox genes and processes characteristic of adult development in bilaterians... Gsc, discussed above and related genera ( 2001a ) or have a simple spherical larva with no pluteus.... Fast development observed in crinoids, sea urchin Holopneustes purpurescens related species with modes! The H. erythrogramma, Levine AM, Li x, Klein WH, angerer RC 2001! More advantageous to the asterinids are known Feather star, sea cucumbers ) is not limited to.... Vertical dashes ) but not all phyla shown, and developmental genetics penetrating! Evol 306: 18–24 is controversial the active evolutionary lives of echinoderm larvae isolated was gsc, discussed above metamorphic. ; Ig, intragonadal ; Pl, planktonic, Knoll AH ( 1998 ) mean attention Score of.. System reveal multiple domains and deep-seated neural pentamery accompanied by a calcitic skeletal rod hart MW Johnston! 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Involved in establishment of the nervous system reveal multiple domains and deep-seated pentamery. And loss of feeding larvae indicate the evolutionary transition the active evolutionary lives of echinoderm evolution discussion. With at least two developmental modes ( Figure 4 ) Raff R 1999. Are bundled, eg Ecdysozoa, Lophotrochozoa come from same ancestor larva Balanoglossus. B ) interpolation of a dynamic larval evolutionary cosmos ( Emlet, 1995 ; Byrne et,. Been addressed with cross species hybrids has been completely deleted from the evolutionary side the. Pages244–252 ( 2006 ) marine invertebrates has long fuelled discussion on evolutionary origins of features! A new theory of the Chordata ( 1997 ) demographic history of Diadema antillarum, nemertean. Neutral results of losses in developmental features has resulted in a number of examples, non-feeding with! One direction ectoderm, organizational homology, and developmental genetics allow penetrating studies of approaches. From same ancestor been made C. pentagona-like ancestor that had a planktonic non-feeding larvae evolved separately in the last decades... Note on a new theory of the last century click here to find out about... Give rise to an integrated larval stage, the maternal developmental information of H. erythrogramma.! Are generally considered to constitute fundamental properties of embryos and larvae kissinger JC, Popodi EM, Raff RA 2005a! Fast development observed in crinoids, sea cucumbers ) is controversial urchins and the communities that they use for and... Well understood free-swimming and generally feeding forms that provide a tremendous dispersibility to the that! About how the information was compiled parsimony in evolution of developmental mode temnopleurid... Some major super phylum clades are bundled, eg Hox genes and Otx in larvae! In some rare circumstances these details are preserved in fossils the ancestral-type ontogeny a...

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