CHAPTER 32AN INTRODUCTION TO ANIMAL EVOLUTION

-What is an Animal?

-Two Views of Animal Diversity

-The Origins of Animal Diversity

Animal life began  in Precambrian seas with the evolution of multicellular forms that lived by eating other organisms. This new way of life allowed the exploitation of previously untapped resources and led to an evolutionary radiation of diverse forms. Early animals populated the seas, fresh water, and eventually the land. In the above photo of a coral reef, the diver, the fish, and the various invertebrates (animals without backbones) are just a few examples of the diverse forms derived during the past half-billion years of animal evolution .

This chapter begins with the general characteristics of animals. We then discuss possible relationships among the animal phyla and examine hypotheses about the origin and early diversification of animals. This overview provides an orientation for our closer look at animal phyla in the next two chapters .

WHAT IS AN ANIMAL? Structure, nutrition, and life history define animals

Constructing a good definition of an animal is not as easy as it might first appear.

There are exceptions to nearly every criterion for distinguishing an animal from other life forms.

However, when taken together, the following characteristics of animals will serve our purposes.

1. Animals are multicellular, heterotrophic eukaryotes.

In contrast to the autotrophic nutrition of plants and algae, animals must take into their bodies preformed organic molecules; they cannot construct them from inorganic chemicals.

Most animals do this by ingestion--eating other organisms or organic material that is decomposing.

2. Animal cells lack the cell walls that provide strong support in the bodies of plants and fungi.

The multicellular bodies of animals are held together by structural proteins, the most abundant being collagen.

In addition to collagen, which is found mainly in extracellular matrices, animal tissues have unique types of intercellular junctions--tight junctions, desmosomes, and gap junctions--that are composed of other structural proteins.

3. Also unique among animals are two types of tissues responsible for impulse conduction and movement: nervous tissue and muscle tissue.

4. A few key features of life history also distinguish animals. Most animals reproduce sexually, with the diploid stage usually dominating the life cycle. In most species, a small flagellated sperm fertilizes a larger, nonmotile egg to form a diploid zygote. The zygote then undergoes cleavage, a succession of mitotic cell divisions. During the development of most animals, cleavage leads to the formation of a multicellular stage called a blastula, which in many animals takes the form of a hollow ball. Following the blastula stage is the process of gastrulation, during which layers of embryonic tissues that will develop into adult body parts are produced. The resulting developmental stage is called a gastrula.

Some animals develop directly through transient stages of maturation into adults, but the life cycles of many animals include larval stages. The larva is a sexually immature form. It is morphologically distinct from the adult stage, usually eats different food, and may even have a different habitat than the adult, as in the case of a frog tadpole. Animal larvae eventually undergo metamorphosis, a resurgence of development that transforms the animal into an adult.

IncompleteMetamorphosis

CompleteMetamorphosis

5. The transformation of a zygote to an animal of specific form depends on the controlled expression in the developing embryo of special regulatory genes called Hox genes. All eukaryotes have genes that regulate the expression of other genes. And many of these regulatory genes contain common "modules" of DNA sequences called homeoboxes. But among eukaryotes outside the animal kingdom, homeoboxes are not found in homeotic genes, those regulatory genes that function in the development of body form.

So far, genes that are both homeobox-containing in structure and homeotic in function--Hox genes—have been discovered only in animals.

And all animals, from the simplest sponges to the most complex insects and vertebrates, have Hox genes containing homeoboxes of DNA sequences that are clearly related.

In general, the number of Hox genes is correlated with the complexity of the animal’s anatomy.

More specifically, variation in when and where the various Hox genes are expressed in a developing embryo provides the genetic basis for the great diversity of animal forms that have evolved from a common ancestor.

The animal kingdom probably evolved from a colonial, flagellated protist

Most systematists now agree that the animal kingdom is monophyletic; that is, if we could trace all animal lineages back to their origin, they would converge on a common ancestor.

That ancestor was most likely a colonial flagellated protist that lived over 700 million years ago in the Precambrian era.

This protist was probably related to choanoflagellates, a group that arose about a billion years ago.

Modern choanoflagellates are tiny, stalked organisms inhabiting shallow ponds, lakes, and marine environments.

The figure below diagrams one hypothesis for how such an ancestor may have evolved into simple animals with specialized cells arranged in two or more layers.

TWO VIEWS OF ANIMAL DIVERSITY

Zoologists recognize about 35 phyla of animals, though our survey of animal diversity will include only 15 of these major animal groups.

For the past century, there was broad consensus among systematists for at least the major branching in a hypothetical tree of the animal kingdom.

This traditional tree was based mainly on the anatomical features of the animals and on certain details of their embryonic development.

However, the molecular systematics of the past decade is challenging some of these long-held ideas about the phylogenetic relationships among the animal phyla.

The traditional phylogenetic tree of animals is based mainly on grades in body "plans"

This diagram illustrates a phylogenetic tree in which relationships among the animal phyla are based mainly on key characteristics of body plan and embryonic development.

Each major branch represents what systematists call a grade, which is defined by certain body-plan features shared by the animals belonging to that branch.

The circled numbers on the tree mark four deep branch points distinguishing the major grades.

For example, the first branch point splits the grade of animals with no true tissues (the parazoa) from the grade of animals with true tissues (the eumetazoa).

Let’s take a closer look at how the diverse body plans of animals can be organized into grades by focusing on each of these four main dichotomies (branchings).

A traditional view of animal diversity based on body-plan grades. The circled numbers key four main branch points to the headings and discussion in the text. The branches with broken lines indicate relationships that are unresolved based on anatomy and embryology.

The Parazoa-Eumetazoa Dichotomy

Among the extant phyla, sponges (phylum Porifera) represent an early branch of the animal kingdom.

Sponges have unique development and a structural simplicity that separates them from all other animal phyla.

They lack true tissues and are called the parazoans (meaning "beside the animals").

Tissues are a basic feature of nearly all other animal phyla, collectively called the eumetazoans.

The Radiata-Bilateria Dichotomy

The eumetazoans are divided into two major branches, partly on the basis of body symmetry.

Members of phylum Cnidaria (hydras; jellies, also called "jellyfishes"; sea anemones; and their relatives) and phylum Ctenophora (comb jellies) have radial symmetry (FIGURE 32.5a) and are collectively called radiata.

A radial animal has a top and bottom, or an oral (mouth) and an aboral side, but no head end and rear end and no left and right.

The other major branch of eumetazoan evolution led to animals with bilateral (two-sided) symmetry .

A bilateral animal has not only a dorsal (top) side and a ventral (bottom) side, but also an anterior (head) end and a posterior (tail) end and a left and right side.

Animals of this body-plan grade are collectively called bilateria.

Body symmetry. The pail and shovel are included to help you remember the radial-bilateral distinction. (a) The parts of a radial animal, such as this sea anemone (phylum Cnidaria), radiate from the center. Any imaginary slice through the central axis would divide the animal into mirror images. (b) A bilateral animal, such as a lobster (phylum Arthropoda), has a left and right side. Only one imaginary cut would divide the animal into mirror-image halves.

Associated with bilateral symmetry is cephalization, an evolutionary trend toward the concentration of sensory equipment on the anterior end, the end of a traveling animal that is usually first to encounter food, danger, and other stimuli. In most bilateral animals, cephalization also includes the development of a central nervous system concentrated in the head and extending toward the tail as a longitudinal nerve cord.

A head end is an adaptation for movement, such as crawling, burrowing, or swimming.

The symmetry of an animal generally fits its lifestyle.

Many radial animals are sessile forms (attached to a substratum) or plankton (drifting or weakly swimming aquatic forms).

Their symmetry equips them to meet the environment equally well from all sides.

Most animals that move actively from place to place are bilateral.

These two fundamentally different kinds of symmetry probably arose very early in the history of animal life.

Another difference in body plan helps define the radiata-bilateria split: In all animals except sponges, the embryo becomes layered through the process of gastrulation.

As development progresses, these concentric layers, called germ layers, form the various tissues and organs of the body.

Ectoderm, covering the surface of the embryo, gives rise to the outer covering of the animal and, in some phyla, to the central nervous system.

Endoderm, the innermost germ layer, lines the developing digestive tube, or archenteron, and gives rise to the lining of the digestive tract and organs derived from it, such as the liver and lungs of vertebrates.

All eumetazoans except cnidarians and ctenophores (the radiata) have a third germ layer, the mesoderm, between the ectoderm and endoderm.

Mesoderm forms the muscles and most other organs between the digestive tube and the outer covering of the animal.

Cnidarians and ctenophores have only two germ layers (ectoderm and endoderm) or have a third layer that is not homologous with the mesoderm of bilateral animals.

As a group, the radiata are said to be diploblastic (having two germ layers).

All other eumetazoans, the bilateria, are triploblastic (having three germ layers).

The Acoelomate, Pseudocoelomate, and Coelomate Grades

Triploblastic animals with solid bodies--that is, without a cavity between the digestive tract and outer body wall--are collectively called acoelomates (from the Greek a , without, and koilos , a hollow).

This group includes phylum Platyhelminthes, the flatworms.

In contrast to the acoelomates, most phyla of bilateral, triploblastic animals have tube-within-a-tube body plans, with a body cavity, a fluid-filled space separating the digestive tract from the outer body wall.

Body plans of the bilateria. The various organ systems of the animal develop from the three germ layers that form in the embryo. Colors traditionally used to represent the germ layers and their derivatives are blue for ectoderm, red for mesoderm, and yellow for endoderm.

Among animals with a body cavity, there are differences in how the cavity develops.

If the cavity is not completely lined by tissue derived from mesoderm, it is termed a pseudocoelom.

Animals with this body plan, such as rotifers (phylum Rotifera) and roundworms (phylum Nematoda), are called pseudocoelomates.

Coelomates are animals with a true coelom, a fluid-filled body cavity completely lined by tissue derived from mesoderm.

The inner and outer layers of tissue that surround the cavity connect dorsally and ventrally to form mesenteries, which suspend the internal organs.

A body cavity has many functions.

Its fluid cushions the suspended organs, helping to prevent internal injury. In soft-bodied coelomates such as earthworms, the noncompressible fluid of the body cavity is under pressure and functions as a hydrostatic skeleton against which muscles can work.

The cavity also enables the internal organs to grow and move independently of the outer body wall.

If it were not for your coelom, every beat of your heart or ripple of your intestine could deform your body surface, and exercise would distort the shapes of the internal organs.

The Protostome-Deuterostome Dichotomy Among Coelomates

The coelomate phyla are divided into two distinct grades: Protostomia and Deuterostomia. Mollusks, annelids, arthropods, and several other phyla represent one of these grades and are collectively called protostomes.

Echinoderms, chordates, and some other phyla, collectively called deuterostomes, represent the other grade.

(Some zoologists include the acoelomates and pseudocoelomates with the protostomes in the traditional phylogenetic tree, but this text uses the term protostome only as a subgroup of coelomate animals.)

Protostomes and deuterostomes are distinguished by several fundamental differences in their development.

Cleavage. The pattern of cleavage divisions during early development generally differs between the two coelomate branches, though there are many exceptions to this distinction.

Many protostomes undergo spiral cleavage, in which planes of cell division are diagonal to the vertical axis of the embryo.

As seen in the eight-cell stage resulting from spiral cleavage, small cells lie in the grooves between larger, underlying cells.

Furthermore, the so-called determinate cleavage of some protostomes rigidly casts the developmental fate of each embryonic cell very early.

A cell isolated at the four-cell stage from a snail, for example, forms an inviable embryo that lacks parts.

A comparison of early development in protostomes and deuterostomes. These are useful general distinctions, though there are many variations and exceptions to these patterns of development.

In contrast to the spiral cleavage pattern, the zygotes of many deuterostomes undergo radial cleavage.

Here, the cleavage planes are either parallel or perpendicular to the vertical axis of the egg; as seen in the eight-cell stage, the tiers of cells are aligned, one directly above the other.

Most deuterostomes are further characterized by indeterminate cleavage, meaning that each cell produced by early cleavage divisions retains the capacity to develop into a complete embryo.

The cleavage of a single mouse embryo in vitro. (A) 2-cell stage. (B) 4-cell stage. (C) Early 8-cell stage. (B) (D) Compacted 8-cell stage. (E) Morula. (F) Blastocyst.

For example, if the cells of a sea star embryo are separated at the four-cell stage, each will go on to form a normal larva.

It is the indeterminate cleavage of the human zygote that makes identical twins possible.

This characteristic also explains the developmental versatility of the embryonic "stem cells" that may provide new ways to overcome a variety of diseases, including juvenile diabetes, Parkinson’s disease, and Alzheimer’s disease (see Chapter 21).

Coelom Formation. Another difference between protostomes and deuterostomes is apparent later in development.

In gastrulation, the developing digestive tube of an embryo initially forms as a blind pouch, the archenteron.

As the archenteron forms in a protostome, initially solid masses of mesoderm split to form the coelomic cavities; this is called schizocoelous development (from the Greek schizo , split).

Development of the body cavities of deuterostomes is termed enterocoelous: The mesoderm buds from the wall of the archenteron and hollows to become the coelomic cavities (FIGURE 32.7b).

Blastopore Fate. A third fundamental difference between protostomes and deuterostomes is in the fate of the blastopore, the opening of the archenteron.

After the archenteron develops, a second opening forms at the opposite end of the gastrula.

Ultimately, the blastopore and this second opening become the two ends of the digestive tube (the mouth and the anus).

The mouth of many protostomes develops from the first opening, the blastopore, and it is for this characteristic that the protostome grade is named (from the Greek protos , first, and stoma , mouth).

In contrast, the mouth of a deuterostome (from the Greek deuteros , second) is derived from the secondary opening, and the blastopore usually forms the anus, not the mouth (FIGURE 32.7c).

Molecular systematists are moving some branches around on the phylogenetic tree of animals

Modern phylogenetic systematics is based on the identification of clades, which are monophyletic sets of taxa as defined by shared-derived characters unique to those taxa and their common ancestor.

Based on cladistic methods, a phylogenetic tree takes shape as a hierarchy of clades nested within larger clades—the finer branches and major branches of the tree, respectively.

The traditional phylogenetic tree of animals is based on the assumption that grades in body plan are good indicators of clades, as long as the key anatomical and embryological homologies that define a grade are unique to the phyla placed on that evolutionary branch.

Molecular systematics has added a new set of shared-derived characters in the form of unique monomer sequences within certain genes and their products.

And these molecular data can be used to identify the clusters of monophyletic taxa that make up clades.

There wouldn’t be much of a story here if molecular systematics simply reinforced the traditional animal tree based on comparative anatomy and embryology.

But that is not the case.

Phylogenetic tree based on small-subunit ribosomal RNA sequences showing three domains of life.

The phylogenetic tree in FIGURE 32.8 is based on nucleotide sequences in the small subunit ribosomal RNA (SSU-rRNA), the gene product that is so commonly analyzed by molecular systematists.

Researchers have also sequenced some of the Hox genes in various animals, and so far those sequences support the phylogenetic tree based on SSU-rRNA analysis.

Let’s examine how this tree agrees with the traditional one, and how the two trees differ.

Animal phylogeny based on sequencing of SSU-rRNA. Note the two distinct clades of protostomes: Lophotrochozoa and Ecdysozoa. And note that these two clades include the acoelomates (Platyhelminthes), the pseudocoelomates (Nematoda and Rotifera), and the lophophorates (Bryozoa, Phoronida, and Brachiopoda).

How Are the Two Views of Animal Phylogeny Alike?

Agreement on the Deepest Branches. First, there is no dispute about the very deepest branches of animal phylogeny.

Molecular systematics supports the traditional hypotheses of the Parazoa-Eumetazoa and Radiata-Bilateria dichotomies (see branch points 1 and 2 in FIGURE 32.4).

Agreement on the Deuterostome Clade. Second, the molecular evidence reinforces the hypothesis that the deuterostomes, which include echinoderms such as sea stars and chordates such as vertebrates, make up a clade--a monophyletic sub-branch of the coelomate bilateria (see branch point 4 in FIGURE 32.4).

How Are the Two Views of Animal Phylogeny Different?

You can see where the traditional and molecular-based phylogenetic trees clash by focusing on the protostome branch of the bilateria as represented in FIGURE 32.8.

Two Main Protostome Clades. First, note that the molecular evidence resolves two distinct clades within the protostomes: Lophotrochozoa, which includes the annelids (segmented worms) and the mollusks (such as clams and snails); and Ecdysozoa, which includes the arthropods.

Based on comparative anatomy and embryology alone, the relationships among the annelids, mollusks, and arthropods were uncertain.

Some zoologists favored an annelid-arthropod lineage, partly because both annelids and arthropods have segmented bodies (think of an earthworm, which is an annelid, and the underside of the tail of a lobster, which is an arthropod).

But other zoologists argued that certain features linked the annelids closer to the mollusks than to the arthropods.

This hypothesis was based in part on the observation that many annelids and mollusks go through a similar larval stage called the trochophore larva

The molecular data add weight to the hypothesis of an annelid-mollusk clade.

Relocation of the Acoelomates and Pseudocoelomates. 

In the grade-based phylogeny of FIGURE 32.4, the acoelomate phylum Platyhelminthes (flatworms) branches from the tree before the origin of body cavities.

But the molecular data place the flatworms among the protostomes, specifically within the lophotrochozoan clade.

If this turns out to be correct, the implication is that flatworms are not the primitive "pre-coelomate" animals of the traditional phylogeny, but are protostomes in which the body plan became simplified by loss of the coelom later in evolution.

Similarly, the molecular-based phylogeny also places the pseudocoelomate phyla Rotifera (rotifers) and Nematoda (nematodes, or round worms) within the protostome clade.

Rotifers cluster with the lophotrochozoan phyla, while nematodes fit among the ecdysozoans.

The name Ecdysozoa refers to a characteristic shared by nematodes, arthropods, and some of the other ecdysozoan phyla (which are not included in our survey).

These animals secrete external skeletons (exoskeletons)--the armor of a lobster is an example.

As the animal grows, it molts, squirming out of its old exoskeleton and secreting a new, larger one.

The shedding of the old exoskeleton is called ecdysis, the process for which the ecdysozoans are named.

Though named for this characteristic, the clade is actually defined mainly by the molecular evidence for common ancestry.

Assignment of the Lophophorate Phyla. 

Among the coelomates are three phyla called the lophophorate phyla.

The animals of these three phyla all have a structure called a lophophore, a horseshoe-shaped crown of ciliated tentacles used for feeding.

The lophophorate phyla share certain characteristics with protostomes and other features with deuterostomes--hence the dashed line indicating uncertain phylogeny in the traditional tree.

A lophophorate. This bryozoan uses its lophophore, the crown of ciliated tentacles, for feeding.

If the molecular data stand up, they settle debate about the affinities of the lophophorate phyla by placing them as protostomes among the lophotrochozoans.

Thus, we can now dissect this long word as the name for a group that unites the lophophore-bearing phyla with phyla having a trochophore larva.

Note, however, that while the name of this clade may be based on anatomical and developmental characteristics, the animals are grouped mainly because they share certain DNA sequences.

Summary of the Two Views of Animal Diversity

We can summarize the differences between the traditional and molecular-based animal phylogenies this way: the molecular data recognize two distinct clades within the protostomes--Lophotrochozoa and Ecdysozoa--and distribute the acoelomates, pseudocoelomates, and lophophorate phyla among those two protostome clades.

Though we will base our survey of animal phyla in the next two chapters on the newer, molecular-based phylogeny, we do so with two caveats.

First, we will not discard the concept of body-plan grades because it is still a very useful way to think about the diversity of animal forms that have evolved.

Second, the phylogenetic tree of animals built from molecular data, like all such trees, represents a set of hypotheses about the history of life, and is thus tentative.

The molecular phylogeny is based on just a very few genes--and mainly on one, the gene for SSU-rRNA.

Many zoologists will probably stick with the grade-based phylogeny unless much more molecular evidence builds a convincing case for a new tree.

In the meantime, the hypothetical tree based on molecules will inform continuing research, including additional studies of anatomy, embryology, cell structure, and other non-molecular analyses.

Ideally, such research will eventually square the molecular data with the data from other approaches.

Continued exploration of the fossil record, of course, will also help to reconstruct the history of the animal kingdom.

But as we’ll see in this chapter’s last major section, there is a reason that it has not been possible so far for paleontologists to sort out the evolutionary relationships among the animal phyla.

THE ORIGINS OF ANIMAL DIVERSITY

Most animal phyla originated in a relatively brief span of geologic time

The fossil record and molecular studies concur that the diversification that produced the many animal phyla occurred rapidly on the vast scale of geologic time.

This relatively brief evolutionary episode probably lasted about 40 million years (about 565 to 525 million years ago) during the late Precambrian and early Cambrian (which began about 543 million years ago).

Paleontologists have named the last period of the Precambrian era the Ediacaran period, for the Ediacara Hills of Australia, where fossils of Precambrian animals were first discovered.

The fossils range in age from about 565 to 543 million years old.

Similar animals of the same vintage have since been found on other continents.

There is some evidence that animal life began earlier, and maybe much earlier.

In 2000, researchers reported the discovery of fossilized animal embryos in Chinese strata that are 570 million years old.

And in 1998, a team of paleontologists discovered what could be fossilized burrows of animals in rocks that are 1.1 billion years old.

By themselves, these putative trace fossils of animals would not convince many biologists to push back the origin of animals so far.

However, the data of molecular systematics also suggest an animal origin about a billion years ago.

That would mean that the genesis of animals was part of an early diversification of multicellular eukaryotes, known mainly from fossils of algae.

Until there is more solid evidence for such ancient animals, however, all we know for sure is that a diversity of animals had evolved by the time of the Ediacaran period.

Most of the Ediacaran fossils appear to represent cnidarians (animals similar to hydras), but soft-bodied mollusks (similar to a modern group called the chitons) were also present, and numerous fossilized burrows and tracks indicate the activities of several forms of worms.

In contrast to the relatively limited variety of Ediacaran animals, nearly all the major animal body plans appear in Cambrian rocks dating from 543 to 525 million years ago.

During this relatively short span, a burst of animal origins calledthe Cambrian explosion left a rich fossil assemblage that includes the first animals with hard, mineralized skeletons (see FIGURE 26.8).

The Burgess Shale in British Columbia, Canada, is the most famous fossil bed documenting the diversity of Cambrian animals.

Two other fossil sites, one in Greenland and the other in the Yunnan region of China, predate the Burgess Shale by more than 10 million years.

Burgess Shale fossils are rather bizarre-looking in the context of the marine animals we know today.

Some of these Cambrian forms may represent extinct "experiments" in animal diversity.

However, most of the Cambrian fossils, as strange as they may appear to us, are simply ancient variations within the taxonomic boundaries of phyla still represented in the modern fauna.

Indeed, the number of exclusively Cambrian phyla seems to be dropping as the fossils are studied more closely and are classified in extant phyla.

On the scale of geologic time, animals diversified so rapidly that it is difficult from the fossil record to sort out the sequence of branching in animal phylogeny.

And that is why, when reconstructing the evolutionary history of animal phyla, systematists depend largely on clues from the comparative anatomy, embryology, developmental genetics, and molecular systematics of extant species.

"Evo-devo" may clarify our understanding of the Cambrian diversification

What sparked the Cambrian explosion?

There are three main hypotheses for what caused the diversification of animals:

1. Ecological Causes : The main variation on this hypothesis emphasizes the emergence during the Cambrian of predator-prey relationships.

Such a change in the dynamics of biological communities would lead to a diversity of evolutionary adaptations such as various kinds of protective shells and diverse modes of locomotion.

2. Geologic Causes : Perhaps, for example, atmospheric oxygen finally reached a high enough concentration during the Cambrian to support the more active metabolism required for the feeding and other activities of mobile animals.

3. Genetic Causes : Much of the diversity in body form we observe among the 35 or so animal phyla is associated with variations in the spatial and temporal expression of Hox genes within developing embryos.

Thus, it is a reasonable hypothesis that the diversification of animals was associated with the evolution of the Hox complex of regulatory genes, which led to variation in morphology during embryonic development.

In fact, the Cambrian explosion is a major interest of many of the biologists working in the field of "evo-devo," the new synthesis of evolutionary biology and developmental biology.

These three major hypothetical causes of the Cambrian explosion are not mutually exclusive.

The relatively rapid radiation of animal phyla over a half-billion years ago may have been a product of multiple causes, both external (geologic change and ecological change) and internal (genetic change).

Apparently, by the end of the Cambrian radiation, the animal phyla were locked into developmental patterns that constrained evolution enough that no additional phyla evolved after that period.

Of course, this does not imply that animal evolution came to a halt; variations in developmental patterns continue to allow subtle changes in body structures and functions, leading to speciation and the origin of taxa below the phylum level.

In the last half-billion years, animal evolution has mainly generated new variations on old "designs."

ANIMAL EVOLUTION

Grade Phylogeny

Molecular Phylogeny