The hidden biology of sponges and ctenophores
2015; Elsevier BV; Volume: 30; Issue: 5 Linguagem: Inglês
10.1016/j.tree.2015.03.003
ISSN1872-8383
AutoresCasey W. Dunn, Sally P. Leys, Steven H. D. Haddock,
Tópico(s)Coral and Marine Ecosystems Studies
Resumo•Ctenophores or sponges are the sister group to all other animals.•Biases hide some complex traits in these animals and make them appear simpler than they are.•These biases supported the misconception that living animals represent grades of complexity.•It is critical to investigate the unique but hidden biology of ctenophores and sponges. Animal evolution is often presented as a march toward complexity, with different living animal groups each representing grades of organization that arose through the progressive acquisition of complex traits. There are now many reasons to reject this classical hypothesis. Not only is it incompatible with recent phylogenetic analyses, but it is also an artifact of 'hidden biology', that is, blind spots to complex traits in non-model species. A new hypothesis of animal evolution, where many complex traits have been repeatedly gained and lost, is emerging. As we discuss here, key details of this new model hinge on a better understanding of the Porifera and Ctenophora, which have each been hypothesized to be sister to all other animals, but are poorly studied and often misrepresented. Animal evolution is often presented as a march toward complexity, with different living animal groups each representing grades of organization that arose through the progressive acquisition of complex traits. There are now many reasons to reject this classical hypothesis. Not only is it incompatible with recent phylogenetic analyses, but it is also an artifact of 'hidden biology', that is, blind spots to complex traits in non-model species. A new hypothesis of animal evolution, where many complex traits have been repeatedly gained and lost, is emerging. As we discuss here, key details of this new model hinge on a better understanding of the Porifera and Ctenophora, which have each been hypothesized to be sister to all other animals, but are poorly studied and often misrepresented. We have two windows on early animal evolution: fossils and living animal diversity. Bringing living animal diversity to bear on our understanding of early animal evolution, events that happened hundreds of millions of years ago, requires analyses of phylogenetic relations between animals and the description of morphological, developmental, genomic, and physiological traits across a broad diversity of living animals. Extensive progress has been made in recent years on animal phylogeny [1Nielsen C. Animal Evolution, Interrelationships of the Living Phyla.3rd edn. Oxford University Press, 2012Google Scholar, 2Wagele J.W. Bartholomaeus T. Deep Metazoan Phylogeny: the Backbone of the Tree of Life. Walter De Gruyter, 2014Crossref Scopus (11) Google Scholar, 3Dunn C.W. et al.Animal phylogeny and its evolutionary implications.Annu. Rev. Ecol. Evol. Syst. 2014; 45: 371-395Crossref Scopus (235) Google Scholar], with particular interest in the deepest relations in the animal tree. All known living animals belong to one of five clades: Porifera (sponges), Ctenophora (comb jellies), Placozoa, Cnidaria, and Bilateria. The monophyly (see Glossary) of each of these clades is broadly supported, but there has been considerable debate about how they are related to each other and, therefore, what the first splits in the animal tree were. Well-sampled recent phylogenetic analyses place either Ctenophora or Porifera as the sister group to the remaining animals (Figure 1). To examine the evolutionary implications of these relations we need more than phylogenies: we also need to describe the biology of these animals so that we can map characters onto the phylogeny and reconstruct their evolutionary history. Unfortunately, ctenophores and sponges are among the least-studied animals and much remains unknown about their morphology, physiology, and molecular biology (Box 1). We know less about their unique complex traits than we do about the unique complex traits of many bilaterians, and our ignorance likely extends to complex traits that have yet to be discovered (Box 1). Making matters worse, what is known about ctenophores and sponges is filtered through the lens of bilaterian biology (Box 1) and often misrepresented (Box 2, Box 3). This leaves considerable gaps in our understanding of traits that are key to reconstructing early animal evolution, and the historical focus on studying complex traits found in Bilateria is often misinterpreted as evidence that there are few unique complex traits found in other animals (Box 1). These gaps must be closed to answer basic questions, such as: what features did the most recent common ancestor of all animals have? In what order and by what mechanisms were complex traits acquired within each lineage? How many times have these traits been gained or lost?Box 1The hidden biology of nonbilateriansAll living animals belong to one of five clades: Porifera, Ctenophora, Placozoa, Cnidaria, and Bilateria. To a first approximation, the study of zoology is the study of Bilateria. Humans and all the best-studied model animal species (mouse, Drosophila melanogaster, Caenorhabditis elegans, and others) are within Bilateria. All of the terrestrial animals, and most freshwater animals that humans regularly encounter are within Bilateria. Most known animal species are within Bilateria (in fact, most known species belong to a single bilaterian clade: Arthropoda). However, if we want to understand the full breadth of animal diversity and the earliest events in animal evolution, we need to study all animals, not just Bilateria.To a large extent, the focus on the study of bilaterians is a resource allocation decisions: zoologists spend more time and money studying bilaterians than they do nonbilaterians because they comprise most living animal species, including ourselves and the animals we are most familiar with. However, this creates a problem: currently, we see most nonbilaterian biology through the filter of bilaterian biology (Figure I). All animal clades have a mix of unique traits and traits that are shared with other animals (Figure IA). It is easier to confirm previously known traits and functions than it is to describe new traits and functions, and most previous studies have been on bilaterians. In addition, many widely used tools and reagents have been optimized for Bilateria. This makes it easier to study the aspects of nonbilaterian biology that are similar to bilaterian biology (Figure IB, gray), than it is to study traits that are only found outside Bilateria (Figure IB, black). The candidate gene approach is a widespread example of this. However, just because it is easiest to study the subset of nonbilaterian biology that is shared with bilaterians does not mean that nonbilaterians only have a subset of bilaterian biology, or that bilaterians are more advanced than other animals. It just means that many of their unique features are currently unknown to us: a 'hidden biology' (Figure I) that we have only the first glimpses of. This hidden biology includes novel structures and functions, facilitated by novel mechanisms, that are not found in bilaterian model species. It also includes novel mechanisms that underlie shared structures and functions. The problems of hidden biology also extend to nonmodel bilaterians, although it is more severe in nonbilaterians.What do we miss by letting so much nonbilaterian biology stay hidden? At best, we miss out on some interesting biology, including unique morphology, developmental mechanisms, and physiology. At worst, we are systematically misled. Unfortunately, this is the case when it comes to understanding early animal evolution. It is tempting to mistake our biased perspective (Figure IB) for the actual distribution of traits (Figure IA), which gives the false impressions that nonbilaterians have only a subset of the traits found in Bilateria and, therefore, that they are 'lower' or 'simpler'. This in turn plays into the misconception that living animal diversity conforms to a linear aristotelian scala naturae, from lower to higher animals, and that animal evolution has proceeded by a step-wise accumulation of complex traits, such that the more distantly an animal is related to Bilateria, the more closely it resembles the most recent common ancestor of all animals. In reality, all living animal lineages have had the same amount of time to evolve since the most recent common ancestor of all animals, and all have gain and lost multiple traits. We need to understand the traits present in all animal groups, not just those that are present in Bilateria, if we are to understand early animal evolution.Box 2CtenophoresClearing up common misconceptions-Ctenophores are usually figured upside down. Cydippid ctenophores do not swim with their mouth downward; they swim with their mouth forward and typically rest with their mouth up. Unlike medusae, which swim with the mouth trailing, ctenophores typically forage and transit mouth first.-Ctenophores share few unique traits with cnidarian medusae, and many of their similarities are superficial and not shared features. For example, most ctenophores and medusae are transparent and gelatinous, but so are many other animals that live in the midwater of the ocean, including salps and pelagic snails.-Ctenophores do not have radial or bilateral symmetry, they have rotational symmetry. There is no plane that divides them into mirror images, as in animals with bilateral or radial symmetry. Instead, any plane that is drawn through the central oral–aboral axis divides a ctenophore into two halves that are the same, just rotated 180 degrees.-Ctenophores are not all pelagic (living in the water column), some are benthic (attached to substrates, with tentacles dangling in the water).-Ctenophores are not 'primitive', 'living fossils', or the ancestors of other living animals. Neither did humans descend from ctenophores.Unique traits and hidden biology-Complex structures made of cilia, including sensory pegs, combs for locomotion, and 'teeth' [24Tamm S.L. Cilia and the life of ctenophores.Invert. Biol. 2014; 133: 1-46Crossref Scopus (60) Google Scholar];-Colloblasts: glue cells found only in ctenophores that are used to capture prey;-Statocysts with unique morphology, function, and development [30Noda N. Tamm S.L. Lithocytes are transported along the ciliary surface to build the statolith of ctenophores.Curr. Biol. 2014; 24: R951-R952Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar];-Rotational symmetry; and-Nervous system components.Box 3SpongesClearing up common misconceptions-Despite frequent assertions to the contrary, sponges do have epithelia. These seal and control ion flow into the mesohyl.-Similarities between choanocytes and choanoflagellates, often cited as evidence of homology of these cell types, are largely superficial. There are many key differences, including the tubulin-dense cytoskeleton of choanoflagellates, the labile microvilli of the collar, and interaction of the collar with the flagellum.-Sponges are often said to lack sensory cells, but cilia that sense and control flow are common across Metazoa, including sponges. Ciliated sensory cells are located on the inside of the osculum. This makes the osculum a sensory organ that provides feedback to the rest of the sponge on water flow through the sponge body. Sponge larvae also have sensory cilia that detect changes in light intensity.-Sponges have behavior, including contractions of myoid cells. It is too slow to be controlled by rapid neurotransmitter-based signaling mechanisms.-Sponges use glutamatergic signaling to coordinate slow contractions, and one group, glass sponges, uses calcium/potassium action potentials for rapid arrest of feeding.-Sponges are not 'primitive', 'living fossils', or the ancestors of other living animals. Neither did humans descend from sponges.Unique traits and hidden biology-Sponges use different minerals (silica or calcium) to build articulated inorganic skeletons comprising spicules. These inorganic mineral skeletons likely arose several times within sponges. Sponges also have organic skeletons, which they use for attachment, support, and even motility.-Sponges have genes representing many of the families of secreted molecules that are specific to the nervous system of other animals, even though sponges do not have nervous systems. This suggests that these molecules have a different function in sponges, and that sponges have a rich but still unknown secretory biology.-Sponges develop two- and three-layered larvae largely via methods of sorting at the individual cell level. Control of animal polarity (a polarized aquiferous system and a polarized larva) may involve Wnt signaling as in other animals, but the role of other metazoan signaling pathways in development is unclear.-Sponges have extensive symbioses with microbes, algae, and other animals (including hydrozoans, zoanthids, and isopods). Both sponges and their symbionts produce an array of metabolites, which have a largely unknown function. All living animals belong to one of five clades: Porifera, Ctenophora, Placozoa, Cnidaria, and Bilateria. To a first approximation, the study of zoology is the study of Bilateria. Humans and all the best-studied model animal species (mouse, Drosophila melanogaster, Caenorhabditis elegans, and others) are within Bilateria. All of the terrestrial animals, and most freshwater animals that humans regularly encounter are within Bilateria. Most known animal species are within Bilateria (in fact, most known species belong to a single bilaterian clade: Arthropoda). However, if we want to understand the full breadth of animal diversity and the earliest events in animal evolution, we need to study all animals, not just Bilateria. To a large extent, the focus on the study of bilaterians is a resource allocation decisions: zoologists spend more time and money studying bilaterians than they do nonbilaterians because they comprise most living animal species, including ourselves and the animals we are most familiar with. However, this creates a problem: currently, we see most nonbilaterian biology through the filter of bilaterian biology (Figure I). All animal clades have a mix of unique traits and traits that are shared with other animals (Figure IA). It is easier to confirm previously known traits and functions than it is to describe new traits and functions, and most previous studies have been on bilaterians. In addition, many widely used tools and reagents have been optimized for Bilateria. This makes it easier to study the aspects of nonbilaterian biology that are similar to bilaterian biology (Figure IB, gray), than it is to study traits that are only found outside Bilateria (Figure IB, black). The candidate gene approach is a widespread example of this. However, just because it is easiest to study the subset of nonbilaterian biology that is shared with bilaterians does not mean that nonbilaterians only have a subset of bilaterian biology, or that bilaterians are more advanced than other animals. It just means that many of their unique features are currently unknown to us: a 'hidden biology' (Figure I) that we have only the first glimpses of. This hidden biology includes novel structures and functions, facilitated by novel mechanisms, that are not found in bilaterian model species. It also includes novel mechanisms that underlie shared structures and functions. The problems of hidden biology also extend to nonmodel bilaterians, although it is more severe in nonbilaterians. What do we miss by letting so much nonbilaterian biology stay hidden? At best, we miss out on some interesting biology, including unique morphology, developmental mechanisms, and physiology. At worst, we are systematically misled. Unfortunately, this is the case when it comes to understanding early animal evolution. It is tempting to mistake our biased perspective (Figure IB) for the actual distribution of traits (Figure IA), which gives the false impressions that nonbilaterians have only a subset of the traits found in Bilateria and, therefore, that they are 'lower' or 'simpler'. This in turn plays into the misconception that living animal diversity conforms to a linear aristotelian scala naturae, from lower to higher animals, and that animal evolution has proceeded by a step-wise accumulation of complex traits, such that the more distantly an animal is related to Bilateria, the more closely it resembles the most recent common ancestor of all animals. In reality, all living animal lineages have had the same amount of time to evolve since the most recent common ancestor of all animals, and all have gain and lost multiple traits. We need to understand the traits present in all animal groups, not just those that are present in Bilateria, if we are to understand early animal evolution. -Ctenophores are usually figured upside down. Cydippid ctenophores do not swim with their mouth downward; they swim with their mouth forward and typically rest with their mouth up. Unlike medusae, which swim with the mouth trailing, ctenophores typically forage and transit mouth first.-Ctenophores share few unique traits with cnidarian medusae, and many of their similarities are superficial and not shared features. For example, most ctenophores and medusae are transparent and gelatinous, but so are many other animals that live in the midwater of the ocean, including salps and pelagic snails.-Ctenophores do not have radial or bilateral symmetry, they have rotational symmetry. There is no plane that divides them into mirror images, as in animals with bilateral or radial symmetry. Instead, any plane that is drawn through the central oral–aboral axis divides a ctenophore into two halves that are the same, just rotated 180 degrees.-Ctenophores are not all pelagic (living in the water column), some are benthic (attached to substrates, with tentacles dangling in the water).-Ctenophores are not 'primitive', 'living fossils', or the ancestors of other living animals. Neither did humans descend from ctenophores. -Complex structures made of cilia, including sensory pegs, combs for locomotion, and 'teeth' [24Tamm S.L. Cilia and the life of ctenophores.Invert. Biol. 2014; 133: 1-46Crossref Scopus (60) Google Scholar];-Colloblasts: glue cells found only in ctenophores that are used to capture prey;-Statocysts with unique morphology, function, and development [30Noda N. Tamm S.L. Lithocytes are transported along the ciliary surface to build the statolith of ctenophores.Curr. Biol. 2014; 24: R951-R952Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar];-Rotational symmetry; and-Nervous system components. -Despite frequent assertions to the contrary, sponges do have epithelia. These seal and control ion flow into the mesohyl.-Similarities between choanocytes and choanoflagellates, often cited as evidence of homology of these cell types, are largely superficial. There are many key differences, including the tubulin-dense cytoskeleton of choanoflagellates, the labile microvilli of the collar, and interaction of the collar with the flagellum.-Sponges are often said to lack sensory cells, but cilia that sense and control flow are common across Metazoa, including sponges. Ciliated sensory cells are located on the inside of the osculum. This makes the osculum a sensory organ that provides feedback to the rest of the sponge on water flow through the sponge body. Sponge larvae also have sensory cilia that detect changes in light intensity.-Sponges have behavior, including contractions of myoid cells. It is too slow to be controlled by rapid neurotransmitter-based signaling mechanisms.-Sponges use glutamatergic signaling to coordinate slow contractions, and one group, glass sponges, uses calcium/potassium action potentials for rapid arrest of feeding.-Sponges are not 'primitive', 'living fossils', or the ancestors of other living animals. Neither did humans descend from sponges. -Sponges use different minerals (silica or calcium) to build articulated inorganic skeletons comprising spicules. These inorganic mineral skeletons likely arose several times within sponges. Sponges also have organic skeletons, which they use for attachment, support, and even motility.-Sponges have genes representing many of the families of secreted molecules that are specific to the nervous system of other animals, even though sponges do not have nervous systems. This suggests that these molecules have a different function in sponges, and that sponges have a rich but still unknown secretory biology.-Sponges develop two- and three-layered larvae largely via methods of sorting at the individual cell level. Control of animal polarity (a polarized aquiferous system and a polarized larva) may involve Wnt signaling as in other animals, but the role of other metazoan signaling pathways in development is unclear.-Sponges have extensive symbioses with microbes, algae, and other animals (including hydrozoans, zoanthids, and isopods). Both sponges and their symbionts produce an array of metabolites, which have a largely unknown function. There are a few reasons why we know so little about sponges and ctenophores, and why what we do know is often confused. First, most research on animals has focused on Bilateria, while other animals have been relatively neglected. Second, this focus on Bilateria makes it easier to study traits in nonbilaterians that are shared with bilaterians than it is to study nonbilaterians traits that are absent in Bilateria. As a result, there is a large amount of hidden biology in nonbilaterians that we know little about (Box 1). This can give the false impression that nonbilaterians have only a subset of features that are also present in bilaterians, and creates a tendency to shoehorn nonbilaterian biology into bilaterian biology. Third, the diversity within Porifera and Ctenophora is chronically underappreciated. There is no typical species: we must study multiple species strategically sampled across each clade. Fourth, most ctenophore and sponge species are fragile and live in marine environments that are difficult and expensive to study. Bilateria is a diverse group and many of its members are also poorly known, but their closer relation to the best-known model animals means that these shortcomings are, in many cases, easier to overcome and do not have as big an impact on our understanding of the earliest events in animal evolution. Here, we summarize key aspects of ctenophore and sponge biology, attempt to dispel some common misconceptions about these animals, and explore several aspects of how a biased perspective on complexity in different animal clades affects our understanding of animal evolution. Until recently, there was consensus that Porifera is the sister group to all other animals and the placement of Ctenophora was treated as an independent question. This placement of sponges was based in large part on the hypothesized homology of choanoflagellates and choanocytes, and on the lack in sponges of complex characters that were hypothesized to be synapomorphies of all other animals. Both these morphological arguments have serious problems on closer examination (see sponge section below). Two hypotheses for the placement of Ctenophora historically have received the most attention [4Wallberg A. et al.The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling.Cladistics. 2004; 20: 558-578Crossref Scopus (74) Google Scholar]: Coelenterata (= Radiata, Figure 1A) [5Hyman L.H. The Invertebrates: Protozoa through Ctenophora. McGraw-Hill, 1940Google Scholar], with Ctenophora as the sister group to Cnidaria, and Acrosomata (Figure 1B) [6Ax P. Das System der Metazoa, Band I. G. Fischer Verlag, 1995Google Scholar], with Ctenophora as the sister group to Bilateria. Proposed Coelenterata synapomorphies, which reflect an attempt to homologize the body plans of cnidarian medusae and ctenophores, include radial symmetry and the presence of two germ layers separated by a gelatinous extracellular matrix [5Hyman L.H. The Invertebrates: Protozoa through Ctenophora. McGraw-Hill, 1940Google Scholar]. These proposed Coelenterata synapomorphies are superficial similarities (see ctenophore section below). For example, ctenophores have rotational symmetry, not radial symmetry, and cnidarians have diverse symmetries [7Dunn C.W. Complex colony-level organization of the deep-sea siphonophore Bargmannia elongata (Cnidaria, Hydrozoa) is directionally asymmetric and arises by the subdivision of pro-buds.Dev. Dyn. 2005; 234: 835-845Crossref PubMed Scopus (35) Google Scholar, 8Manuel M. Early evolution of symmetry and polarity in metazoan body plans.C. R. Biol. 2009; 332: 184-209Crossref PubMed Scopus (66) Google Scholar]. Proposed synapomorphies for Acrosomata include sperm and muscle structure [6Ax P. Das System der Metazoa, Band I. G. Fischer Verlag, 1995Google Scholar], although later work brings these interpretations into question [9Riesgo A. Maldonado M. An unexpectedly sophisticated, V-shaped spermatozoon in Demospongiae (Porifera): reproductive and evolutionary implications.Biol. J. 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U.S.A. 1998; 95: 15458-15463Crossref PubMed Scopus (181) Google Scholar], none have provided strong support for sponges as the sister group to all other animals under all analysis conditions. No molecular studies support Acrosomata, but some have recovered Coelenterata [14Philippe H. et al.Phylogenomics revives traditional views on deep animal relationships.Curr. Biol. 2009; 19: 706-712Abstract Full Text Full Text PDF PubMed Scopus (534) Google Scholar]. Recent studies have instead suggested that ctenophores, not sponges, are the sister group to all other animals (Figure 1C) [15Dunn C.W. et al.Broad phylogenomic sampling improves resolution of the animal tree of life.Nature. 2008; 452: 745-749Crossref PubMed Scopus (1460) Google Scholar, 16Hejnol A. et al.Assessing the root of bilaterian animals with scalable phylogenomic methods.Proc. Biol. 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Phylogenetic analyses of gene gain and loss are consistent with this placement of ctenophores [17Ryan J.F. et al.The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution.Science. 2013; 342: 1242592Crossref PubMed Scopus (453) Google Scholar]. Similar to some earlier studies [13Collins A.G. Evaluating multiple alternative hypotheses for the origin of Bilateria: an analysis of 18S rRNA molecular evidence.Proc. Natl. Acad. Sci. U.S.A. 1998; 95: 15458-15463Crossref PubMed Scopus (181) Google Scholar], these also support a clade comprising Placozoa, Cnidaria, and Bilateria that has been named Parahoxozoa [22Ryan J.F. et al.The homeodomain complement of the ctenophore Mnemiopsis leidyi suggests that Ctenophora and Porifera diverged prior to the ParaHoxozoa.Evodevo. 2010; 1: 9Crossref PubMed Scopus (105) Google Scholar], although parahox genes may not be a synapomorphy of this group [23Fortunato S.A.V. et al.Calcisponges have a ParaHox gene and dynamic expression of dispersed NK homeobox genes.Nature. 2014; 514: 620-623Crossref PubMed Scopus (74) Google Scholar]. It is now clear that the phylogenetic placement of Porifera and Ctenophora are not independent questions, and must be addressed together. Improved sampling of genome sequences, coupled with
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