31.1 What Evidence Indicates the Animals Are Monophyletic?

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1 31.1 What Evidence Indicates the Animals Are Monophyletic? What traits distinguish the animals from the other groups of organisms? In contrast to the Bacteria, Archaea, and most microbial eukaryotes, all animals are multicellular. Animal life cycles feature complex patterns of development from a single-celled zygote into a multicellular adult. In contrast to most plants, all animals are heterotrophs. Animals are able to synthesize very few organic molecules from inorganic chemicals, so they must take in nutrients from their environment. The fungi are also heterotrophs. In contrast to the fungi, however, animals use internal processes to break down materials from their environment into the organic molecules they need most. Most animals ingest food into an internal gut that is continuous with the outside environment, in which digestion takes place. In contrast to plants, most animals can move. Animals must move to find food or bring food to them. Animals have specialized muscle tissues that allow them to move, and many animal body plans are specialized for movement. Animal monophyly is supported by gene sequences and morphology The most convincing evidence that all the organisms considered to be animals share a common ancestor comes from their many shared derived molecular and morphological traits. Many gene sequences, such as the ribosomal RNA genes, support the monophyly of animals. Animals display similarities in the organization and function of their Hox genes. Animals have unique types of junctions between their cells (tight junctions, desmosomes, and gap junctions). Animals have a common set of extracellular matrix molecules, including collagen and proteoglycans. Although there are animals in a few clades that lack one or another of these synapomorphies, these species apparently once possessed the traits and lost them during their later evolution. The ancestor of the animal clade was probably a colonial flagellated protist similar to existing colonial choanoflagellates. The most reasonable current scenario postulates a choanoflagellate lineage in which certain cells within the colony began to be specialized some for movement, others for nutrition, others for reproduction, and so on. Once this functional specialization had begun, cells could have continued to differentiate. Coordination among groups of cells could have improved by means of specific regulatory molecules that guided the differentiation and migration of cells in developing embryos. Such coordinated groups of cells eventually evolved into the larger and more complex organisms that we call animals. More than a million animal species have been named and described, and there are doubtless millions of living species that have yet to be named. The synapomorphies that indicate animal monophyly cannot be used to infer evolutionary relationships among animals, because nearly all animals have them. It just gives clues if an organism is an animal or not. Clues to the evolutionary relationships among animal groups thus must be sought in derived traits that are found in some groups but not in others. Such characteristics can be found in fossils, in patterns of embryonic development, in the morphology and physiology of living animals, in the structure of animal molecules, and in the genomes of animals (for example, in mitochondrial and ribosomal RNA genes). Developmental patterns show evolutionary relationships among animals Differences in patterns of embryonic development traditionally provided some of the most important clues to animal phylogeny, although analyses of gene sequences are now showing that some developmental patterns are more evolutionarily labile than previously thought.

2 The first few cell divisions of a zygote are known as cleavage. In general, the number of cells in the embryo doubles with each cleavage. A number of different cleavage patterns exist among animals. Cleavage patterns are influenced by the configuration of the yolk, the nutritive material that nourishes the growing embryo. In reptiles, for example, the presence of a large body of a cellular yolk within the fertilized egg creates an incomplete cleavage pattern in which the dividing cells form an embryo on top of the yolk mass. In echinoderms such as sea urchins, small yolk particles are evenly distributed throughout the egg cytoplasm, so cleavage is complete, with the fertilized egg cell dividing in an even pattern known as radial cleavage. Radial cleavage is the ancestral condition for eumetazoans, so it is found among many protostomes and diploblastic animals as well as deuterostomes. Spiral cleavage, a complicated derived permutation of radial cleavage, is found among many lophotrochozoans, such as earthworms and clams. Lophotrochozoans with spiral cleavage are thus sometimes known as spiralians. The early branches of the ecdysozoans have radial cleavage, although most ecdysozoans have an idiosyncratic cleavage pattern that is neither radial nor spiral in organization. During the early development of most animals, distinct layers of cells form. These cell layers differentiate into specific organs and organ systems as development continues. The embryos of diploblastic animals have only two of these cell layers: an outer ectoderm and an inner endoderm. The embryos of triploblastic animals have, in addition to ectoderm and endoderm, a third distinct cell layer, the mesoderm, which lies between the ectoderm and the endoderm. The existence of three cell layers is a synapomorphy of triploblastic animals, whereas the paraphyletic diploblastic animals (ctenophores and cnidarians) exhibit the ancestral condition. During early development in many animals, a hollow ball one cell thick indents to form a cup-shaped structure. This process is known as gastrulation. The opening of the cavity formed by this indentation is called the blastopore. The pattern of development after formation of the blastopore has been used to divide the triploblastic animals into two major groups. Among members of the first group, the protostomes, the mouth arises from the blastopore; the anus forms later. This appears to be the derived condition. Among the deuterostomes, the blastopore becomes the anus; the mouth forms later. This is thought to be the ancestral condition. We now know that the developmental patterns of animals are more varied than suggested by this simple dichotomy, but the protostomes and deuterostomes are still recognized as distinct animal clades based upon sequence similarities of their genes.

3 Figure 31.1 A Current Phylogenetic Tree of Animals This phylogenetic tree is used here and in the following two chapters. It presents a current interpretation based primarily on molecular data, which are particularly useful for identifying ancient lineage splits. The traits highlighted by red circles will be explained as you read the chapter; you should review this figure closely after you complete your reading RECAP The animals are thought to be monophyletic because they share many derived traits, including multicellularity, mobility, and a heterotrophic lifestyle based on the ingestion of outside nutrients. Evolutionary relationships among animals are inferred from fossils and from molecular and developmental traits that are shared by different groups of animals What Are the Features of Animal Body Plans? The general structure of an animal, the arrangement of its organ systems, and the integrated functioning of its parts are referred to as its body plan. Although animal body plans are extremely varied, they can be seen as variations on four key features: The symmetry of the body The structure of the body cavity

4 The segmentation of the body External appendages that move the body All of these features affect the way in which an animal moves and interacts with its environment. These four attributes vary across a number of basic animal body plans. The regulatory genes that govern the development of body symmetry, body cavities, segmentation, and appendages are widely shared among the different animal groups. Thus we might expect animals to share body plans. Most animals are symmetrical The overall shape of an animal can be described by its symmetry. An animal is said to be symmetrical if it can be divided along at least one plane into similar halves. Animals that have no plane of symmetry are said to be asymmetrical. Many sponges are asymmetrical, but most other animals have some kind of symmetry, which is governed by the expression of regulatory genes. The simplest form of symmetry is spherical symmetry, in which body parts radiate out from a central point. An infinite number of planes passing through the central point can divide a spherically symmetrical organism into similar halves. Spherical symmetry is widespread among unicellular protists, but most animals possess other forms of symmetry. In organisms with radial symmetry, there is one main axis around which body parts are arranged. Two animal groups ctenophores and cnidarians are composed primarily of radially symmetrical animals. A perfectly radially symmetrical animal can be divided into similar halves by any plane that contains the main axis. However, most radially symmetrical animals including the adults of echinoderms such as sea stars and sand dollars are slightly modified so that fewer planes can divide them into identical halves. Many radially symmetrical animals are sessile (sedentary). Others move slowly, but can move equally well in any direction. Bilateral symmetry is characteristic of animals that move in one direction. A bilaterally symmetrical animal can be divided into mirror-image (left and right) halves by a single plane that passes through the midline of its body. This plane runs from the tip, or anterior of the body to its tail, or posterior. A plane at right angles to the midline divides the body into two dissimilar sides. The back of a bilaterally symmetrical animal is its dorsal surface; the belly, which contains the mouth, is its ventral surface. Bilateral symmetry is strongly correlated with cephalization, which is the concentration of sensory organs and nervous tissues in a head at the anterior end of the animal. Cephalization has been evolutionarily favored because the anterior end of a bilaterally symmetrical animal typically encounters new environments first. The structure of the body cavity influences movement Animals can be divided into three types based on the presence and structure of an internal, fluid-filled body cavity. The structure of an animal s body cavity strongly influences the ways in which it can move. Acoelomate animals such as flatworms lack an enclosed, fluid-filled body cavity. Instead, the space between the gut (derived from endoderm) and the muscular body wall (derived from mesoderm) is filled with masses of cells called mesenchyme. These animals typically move by beating cilia. Body cavities come in two types. Both types lie between the ectoderm and the endoderm; they are differentiated by their relationship to the mesoderm. Pseudocoelomate animals have a body cavity called a pseudocoel, a fluid-filled space in which many of the internal organs are suspended. A pseudocoel is enclosed by muscles (mesoderm) only on its outside; there is no inner layer of mesoderm surrounding the internal organs.

5 Coelomate animals have a coelom, a body cavity that develops within the mesoderm. It is lined with a layer of muscular tissue called the peritoneum, which also surrounds the internal organs. The coelom is thus enclosed on both the inside and the outside by mesoderm. A coelomate animal has better control over the movement of the fluids in its body cavity than a pseudocoelomate animal does. Figure 31.4 Animal Body Cavities (A) Acoelomates do not have enclosed body cavities. (B) Pseudocoelomates have a body cavity enclosed by only one layer of mesoderm, which lies outside the cavity. (C) Coelomates have a peritoneum surrounding the internal organs. The body cavities of many animals function as hydrostatic skeletons. Fluids are relatively incompressible, so when the muscles surrounding them contract, they move to another part of the cavity. If the body tissues around the cavity are flexible, fluids squeezed out of one region can cause some other region to expand. The moving fluids can thus move specific body parts. (You can see how a hydrostatic skeleton works by watching a snail emerge from its shell.) An animal with both circular muscles (encircling the body cavity) and longitudinal muscles (running along the length of the body) has even greater control over its movement. Although the hydrostatic function of fluid-filled body cavities is important, most animals also have hard skeletons that provide protection and facilitate movement. Muscles are attached to those firm structures, which may be inside the animal or on its outer surface (in the form of a shell or cuticle). Segmentation improves control of movement Many animals have bodies that are divided into segments. Segmentation facilitates specialization of different body regions. Segmentation also allows an animal to alter the shape of its body in complex ways and to control its movements precisely. If an animal s body is segmented, muscles in each individual segment can change the shape of that segment independently of the others. In only a few segmented animals is the body cavity separated into discrete compartments, but even partly separated compartments allow better control of movement. As we will see, segmentation evolved independently several different times in both the protostomes and the deuterostomes. In some animals, segments are not apparent externally (as in the segmented vertebrae of vertebrates). In other animals, such as the annelids, similar body segments are repeated many times; and in yet other animals, including most arthropods, the segments are visible but differ strikingly. As we will describe in the next chapter, the dramatic evolutionary radiation of the arthropods (including the insects, spiders, centipedes, and crustaceans) was based on changes in a segmented body plan that features muscles attached to the inner surface of an external skeleton, along with a variety of external appendages that move these animals. Appendages enhance locomotion

6 Getting around under their own steam is important to many animals. It allows them to obtain food, to avoid predators, and to find mates. Even some sessile species, such as sea anemones, have larval stages that use cilia to swim, thus increasing the animal s chances of finding a suitable habitat to settle on. Appendages that project externally from the body greatly enhance an animal s ability to move around. Many echinoderms, including sea urchins and sea stars, have myriad tube feet that allow them to move slowly across the substratum. Highly controlled, rapid movement is greatly enhanced in animals whose appendages have become modified into specialized limbs. In two animal groups, the arthropods and the vertebrates, the presence of jointed limbs has been a prominent factor in their evolutionary success. In several independent instances among the arthropod insects, the pterosaurs, the birds, and the bats body plans emerged in which limbs were modified into wings, allowing animals to take to the air RECAP The body plans of animals are all variations on patterns of symmetry, body cavities, segmentation, and appendages. All four can have bearing on movement and locomotion, which are important aspects of the animal way of life What Are the Major Groups of Animals? The Bilateria is a large monophyletic group embracing all animals other than sponges, ctenophores, and cnidarians. The traits that support the monophyly of Bilateria are bilateral symmetry, three cell layers, and the presence of at least seven Hox genes. The bilaterian animals comprise the two major categories mentioned earlier in this chapter, and are classified as either protostomes or deuterostomes. These two groups have been evolving separately for over 500 million years, since the early Cambrian or late Precambrian. The remainder of this chapter describes those animal groups that are not bilaterians. The simplest animals, the sponges, have no cell layers and no organs. Sponges are not a clade, but the name is used for three groups that exhibit the ancestral body organization of animals. All other animals, including the bilatarians, are known as eumetazoans. They have obvious body symmetry, a gut, a nervous system, special types of cell junctions, and well-organized tissues in distinct cell layers (although there have been secondary losses of some of these structures in some eumetazoans). Sponges lack all these features. Sponges are loosely organized animals Sponges are the simplest of animals. They have some specialized cells, but no distinct cell layers and no true organs. Early naturalists thought that they were plants because they lacked body symmetry. Sponges have hard skeletal elements called spicules, which may be small and simple or large and complex. Recent analyses of ribosomal RNA genes suggest that there are three major groups of sponges, which are paraphyletic with respect to the remaining animals. Members of two groups (glass sponges and demosponges) have skeletons composed of silicaceous spicules made of hydrated silicon

7 dioxide. These spicules are remarkable in having greater flexibility and toughness than synthetic glass rods of similar length. Members of the third group, the calcareous sponges, take their name from their calcium carbonate skeletons. It is the latter group that is most closely related to the eumetazoans. The body plan of sponges of all three groups even large ones, which may reach a meter or more in length is an aggregation of cells built around a water canal system. Water, along with any food particles it contains, enters the sponge by way of small pores and passes into the water canals, where choanocytes capture food particles. A skeleton of simple or branching spicules, and often a complex network of elastic fibers, supports the bodies of most sponges. Sponges also have an extracellular matrix, composed of collagen, adhesive glycoproteins, and other molecules, that holds the cells together. Most species are filter feeders; a few species are carnivores that trap prey on hook-shaped spicules that protrude from the body surface. Most of the 8,000 species of sponges are marine animals; only about 50 species live in fresh water. Sponges come in a wide variety of sizes and shapes that are adapted to different movement patterns of water. Sponges living in intertidal or shallow subtidal environments with strong wave action are firmly attached to the substratum. Most sponges that live in slowly flowing water are flattened and are oriented at right angles to the direction of current flow. They intercept water and the prey it contains as it flows past them. Sponges reproduce both sexually and asexually. In most species, a single individual produces both eggs and sperm, but individuals do not self-fertilize. Water currents carry sperm from one individual to another. Asexual reproduction is by budding and fragmentation. Ctenophores are radially symmetrical and diploblastic The ctenophores, also known as the comb jellies, lack most of the Hox genes possessed by all other eumetazoans. Ctenophores have a radially symmetrical, diploblastic body plan, with the two cell layers separated by a thick, gelatinous mesoglea. They have low metabolic rates because the mesoglea is an inert extracellular matrix. Ctenophores have a complete gut, with an entrance and an exit. Food enters through a mouth, and wastes are eliminated through two anal pores. Ctenophores have eight comblike rows of fused plates of cilia, called ctenes. A ctenophore moves through the water by beating these cilia rather than by muscular contractions. Its feeding tentacles are covered with cells that discharge adhesive material when they contact prey. After capturing its prey, a ctenophore retracts its tentacles to bring the food to its mouth. In some species, the entire surface of the body is coated with sticky mucus that captures prey. All of the 100 known species of ctenophores eat small planktonic organisms. They are common in open seas. Cnidarians are specialized carnivores One branch of the next split in the animal lineage led to the cnidarians (jellyfishes, sea anemones, corals, and hydrozoans). The mouth of a cnidarian is connected to a blind sac called the gastrovascular cavity (thus it does not have a complete gut). The gastrovascular cavity functions in digestion, circulation, and gas exchange, and it also acts as a hydrostatic skeleton. The single opening serves as both mouth and anus. The life cycle of most cnidarians has two distinct stages, one sessile and the other motile. In the sessile polyp stage, a cylindrical stalk is attached to the substratum. Individual polyps may reproduce asexually by budding, thereby forming a colony. The motile medusa (plural medusae) is a freeswimming stage shaped like a bell or an umbrella. It typically floats with its mouth and feeding tentacles facing downward. Medusae of many species produce eggs and sperm and release them into

8 the water. A fertilized egg develops into a free-swimming, ciliated larva called a planula, which eventually settles to the bottom and develops into a polyp. Figure The Cnidarian Life Cycle Has Two Stages The life cycle of a scyphozoan (jellyfish) exemplifies the typical cnidarian body forms: the sessile, asexual polyp; and the motile, sexual medusa. Cnidarians have epithelial cells with muscle fibers whose contractions enable the animals to move, as well as simple nerve nets that integrate their body activities. They also have specialized structural molecules (collagen, actin, and myosin) and Hox genes. They are specialized carnivores, using the toxin in their nematocysts to capture relatively large and complex prey. Some cnidarians, including corals and anemones, gain additional nutrition from photosynthetic protists that live in their tissues. Cnidarians, like ctenophores, are largely made up of inert mesoglea. They have low metabolic rates and can survive in environments where they encounter prey only infrequently. Of the roughly 11,000 cnidarian species living today, all but a few live in the oceans. The smallest cnidarians can hardly be seen without a microscope; the largest known jellyfish is 2.5 meters in diameter. We will describe three clades of cnidarians that have many species: the scyphozoans, anthozoans, and hydrozoans. SCYPHOZOANS The several hundred species of scyphozoans are all marine. The mesoglea of their medusae is thick and firm, giving rise to their common name jellyfishes or sea jellies. The medusa rather than the polyp dominates the life cycle of scyphozoans. An individual medusa is male or female, releasing eggs or sperm into the open sea. The fertilized egg develops into a small planula larva that quickly settles on a substratum and develops into a small polyp. This polyp feeds and grows and may produce additional polyps by budding. After a period of growth, the polyp begins to bud off small medusae, which feed, grow, and transform themselves into adult medusa.

9 ANTHOZOANS Members of the anthozoan clade include sea anemones, sea pens, and corals. Sea anemones, all of which are solitary, are widespread in both warm and cold ocean waters. Sea pens, by contrast, are colonial. Each colony consists of at least two different kinds of polyps. The primary polyp has a lower portion anchored in the bottom sediment and a branched upper portion, which projects above the substratum. Along the upper portion, the primary polyp produces smaller secondary polyps by budding. Some of these secondary polyps differentiate into feeding polyps; others circulate water through the colony. Corals also are sessile and colonial. The polyps of most corals form a skeleton by secreting a matrix of organic molecules on which they deposit calcium carbonate, which forms the eventual skeleton of the coral colony. As the colony grows, old polyps die but their calcium carbonate skeletons remain. The living members form a layer on top of a growing bank of skeletal remains, eventually forming chains of islands and reefs. The common names of coral groups horn corals, brain corals, staghorn corals, and organ pipe corals, among others describe their appearance. Corals flourish in clear, nutrient-poor tropical waters. They can grow rapidly in such environments because unicellular photosynthetic protists live endosymbiotically within their cells. These protists provide the corals with products of photosynthesis; the corals, in turn, provide the protists with nutrients and a place to live. This endosymbiotic relationship explains why reef-forming corals are restricted to clear surface waters, where light levels are high enough to support photosynthesis. Coral reefs throughout the world are threatened both by global warming, which is raising the temperatures of shallow tropical ocean waters, and by polluted runoff from development on adjacent shorelines. An overabundance of nitrogen in the runoff gives an advantage to algae, which overgrow and eventually smother the corals. HYDROZOANS Hydrozoans have diverse life cycles. The polyp typically dominates the life cycle, but some species have only medusae; others have only polyps. Most hydrozoans are colonial. A single planula larva eventually gives rise to a colony of many polyps, all interconnected and sharing a continuous gastrovascular cavity. Within such a colony some polyps have tentacles with many nematocysts; they capture prey for the colony. Others lack tentacles and are unable to feed, but are specialized for the production of medusae. Still others are fingerlike and defend the colony with their nematocysts.

10 Figure Hydrozoans Often Have Colonial Polyps The polyps within a hydrozoan colony may differentiate to perform specialized tasks. In the species whose life cycle is diagrammed here, the medusa is the sexual reproductive stage, producing eggs and sperm in organs called gonads RECAP The bilaterian animals fall into two major clades, the protostomes and the deuterostomes. The nonbilateran animals the sponges, cteno-phores, and cnidarians have relatively simple structures and correspondingly simple feeding strategies 31.1 Most animals share a set of derived traits not found in other groups of organisms. These traits include similarities in their ribosomal RNA and Hox genes, cell junctions, and an extracellular matrix. Patterns of embryonic development provide important clues to the evolutionary relationships among animals. Diploblastic animals develop two embryonic cell layers; triploblastic animals develop three. Differences in patterns of early development also characterize two major clades of triploblastic animals, the protostomes and deuterostomes. 31.2

11 Animal body plans can be described in terms of symmetry, body cavity structure, segmentation, and appendages. A few animals have spherical symmetry, but most animals have either radial or bilateral symmetry. Most animals with radial symmetry move slowly or not at all, while animals with bilateral symmetry are able to move more rapidly. Many bilaterally symmetrical animals are cephalized, with sensory and nervous tissues in an anterior head. On the basis of their body cavity structure, animals can be described as acoelomates, pseudocoelomates, or coelomates. Segmentation, which takes many forms, improves control of movement, especially if the animal also has appendages. Parasites have complex life cycles that may involve one or more hosts and several larval stages. A characteristic of an animal or a life cycle stage may improve its performance in one activity, but reduce its performance in another, a situation known as a trade-off All animals other than sponges, ctenophores, and cnidarians belong to a large monophyletic group called the Bilateria. The clade Eumetazoa embraces all animals other than sponges. Sponges are simple animals that lack cell layers and true organs. They have skeletons made up of silicaceous or calcareous spicules. They create water currents and capture food with flagellated feeding cells called choanocytes. Choanocytes are an evolutionary link between the animals and choanoflagellate protists. The ctenophores and cnidarians are diploblastic, radially symmetrical animals. The two cell layers of ctenophores are separated by an inert extracellular matrix called mesoglea. They move by beating fused plates of cilia called ctenes. The life cycle of cnidarians has two distinct stages: a sessile polyp stage and a motile medusa. A fertilized egg develops into a free-swimming planula larva, which settles to the bottom and develops into a polyp.

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