On the Origin of Phyla

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Overview


Owing its inspiration and title to On the Origin of Phlya, James W. Valentine's ambitious book synthesizes and applies the vast treasury of theory and research collected in the century and a half since Darwin's time. By investigating the origins of life's diversity, Valentine unlocks the mystery of the origin of phyla.

One of the twentieth century's most distinguished paleobiologists, Valentine here integrates data from molecular genetics, evolutionary developmental biology, embryology, comparative morphology, and paleontology into an analysis of interest to scholars from any of these fields. He begins by examining the sorts of evidence that can be gleaned from fossils, molecules, and morphology, then reviews and compares the basic morphology and development of animal phyla, emphasizing the important design elements found in the bodyplans of both living and extinct phyla. Finally, Valentine undertakes the monumental task of developing models to explain the origin and early diversification of animal phyla, as well as their later evolutionary patterns.

Truly a magnum opus, On the Origin of Phyla will take its place as one of the classic scientific texts of the twentieth century, affecting the work of paleontologists, morphologists, and developmental, molecular, and evolutionary biologists for decades to come.

"A magisterial compendium . . . . Valentine offers a judicious evaluation of an astonishing array of evidence."—Richard Fortey, New Scientist

"Truly a magnum opus, On the Origin of Phyla has already taken its place as one of the classic scientific texts of the twentieth century, affecting the work of paleontologists, morphologists, and developmental, molecular, and evolutionary biologists for decades to come."—Ethology, Ecology & Evolution

"Valentine is one of the Renaissance minds of our time. . . . Darwin wisely called his best-known work On the Origin of the Species; the origin of the phyla is an even stickier problem, and Valentine deserves credit for tackling it at such breadth . . . . A magnificient book."—Stefan Bengtson, Nature 

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Editorial Reviews

New Scientist - Richard Fortey

"Valentine brings together a mass of evidence from many sources in a magisterial compendium. . . . There is direct evidence from the fossil record, of course. But there is also new evidence from trees of relationships derived from studying similarities in gene sequences of living animals. These are often ambiguous. Then there is evidence from the way genes are expressed during the growth and development of the body plans of animals. . . . Add to this classical morphology and embryology. . . . It is an astonishing range of information all brought together within one pair of covers. It's enough to make mere mortals awestruck. . . . Valentine [offers] a judicious evaluation of an astonishing array of evidence."

Science - R. Andrew Cameron

"A likely candidate for the bookshelves of those who hunt for pre-Cambriam fossils or the historical patterns in DNA sequences."

Nature - Stefan Bengtson

"Valentine [is] one of the Renaissance minds of our time. . . . Darwin wisely called his best-known work On the Origin of Species; the origin of phyla is an even stickier problem, and Valentine deserves credit for tackling it at such breadth. . . . A magnificent book."—Stefan Bengtson, Nature

Trends in Ecology and Evolution - Alessandro Minelli

"Valentine has indeed produced a wonderfully informative and well-written book by mixing together three basic ingredients that are now available: paleontology, molecular phylogeny, and developmental genetics."

Evolution & Development - Rudolf A. Raff

"Valentine envisions the study of the origins of phyla as a multidisciplinary investigation of patterns and process. His book provides a masterful guide to what we know about the origins of the phyla and current research issues relating to the early history of animal life. . . . Valentine does not hesitate to speak his mind, which gives the book a forceful discussion of well-argued ideas."

Quarterly Review of Biology - Francisco J. Ayala

"A magnificent book--authoritative, rich with relevant knowledge, and clearly written. It may be many years before it will be surpassed by any other treatise on the subject."

New Scientist
Valentine brings together a mass of evidence from many sources in a magisterial compendium. . . . There is direct evidence from the fossil record, of course. But there is also new evidence from trees of relationships derived from studying similarities in gene sequences of living animals. These are often ambiguous. Then there is evidence from the way genes are expressed during the growth and development of the body plans of animals. . . . Add to this classical morphology and embryology. . . . It is an astonishing range of information all brought together within one pair of covers. It's enough to make mere mortals awestruck. . . . Valentine [offers] a judicious evaluation of an astonishing array of evidence.

— Richard Fortey

Science
A likely candidate for the bookshelves of those who hunt for pre-Cambriam fossils or the historical patterns in DNA sequences.

— R. Andrew Cameron

Nature
Valentine [is] one of the Renaissance minds of our time. . . . Darwin wisely called his best-known work On the Origin of Species; the origin of phyla is an even stickier problem, and Valentine deserves credit for tackling it at such breadth. . . . A magnificent book.—Stefan Bengtson, Nature

— Stefan Bengtson

Trends in Ecology and Evolution
Valentine has indeed produced a wonderfully informative and well-written book by mixing together three basic ingredients that are now available: paleontology, molecular phylogeny, and developmental genetics.

— Alessandro Minelli

Evolution & Development
Valentine envisions the study of the origins of phyla as a multidisciplinary investigation of patterns and process. His book provides a masterful guide to what we know about the origins of the phyla and current research issues relating to the early history of animal life. . . . Valentine does not hesitate to speak his mind, which gives the book a forceful discussion of well-argued ideas.

— Rudolf A. Raff

Fossil News

"To say that this book--which summarizes the current state of knowledge on how basic animal body plans evolved . . . represents a monumental undertaking is surely understatement of the finest variety. . . . All who study the history of life would benefit from an understanding of the material presented here."—Fossil News

Quarterly Review of Biology
A magnificent book—authoritative, rich with relevant knowledge, and clearly written. It may be many years before it will be surpassed by any other treatise on the subject.

— Francisco J. Ayala

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Product Details

  • ISBN-13: 9780226845494
  • Publisher: University of Chicago Press
  • Publication date: 7/1/2006
  • Edition description: 1
  • Pages: 608
  • Product dimensions: 7.00 (w) x 10.00 (h) x 1.50 (d)

Meet the Author


James W. Valentine is professor emeritus of integrative biology and is affiliated with the Museum of Paleontology and the Center for Integrative Genomics at the University of California, Berkeley. He is the author of Evolutionary Paleoecology of the Marine Biosphere, coauthor of Evolution and Evolving, and editor of Phanerozoic Diversity Patterns: Profiles in Macroevolution.
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Read an Excerpt

ON THE ORIGIN OF PHYLA

By JAMES W. VALENTINE
The University of Chicago Press
Copyright © 2004 The University of Chicago
All right reserved.

ISBN: 978-0-226-84548-7



Chapter One
The Nature of Phyla

Phyla Are Morphologically Based Branches of the Tree of Life

Concepts of Animal Phyla Have Developed over Hundreds of Years

Classifications of organisms in hierarchical systems were in use by the seventeenth and eighteenth centuries. Usually organisms were grouped according to their morphological similarities as perceived by those early workers, and those groups were then grouped according to their similarities, and so on, to form a hierarchy. Thus species, which form the lowest level in the hierarchy, have membership in each of a series of increasingly inclusive hierarchical levels or categories. By an international agreement first formalized in 1901, the tenth edition of Linnaeus's Systema Naturae (1758) was taken as the starting point for priority in zoological nomenclature for taxa in the lower categories. However, there are no international rules for the nomenclature of orders, classes, or phyla. Linnaeus himself used five hierarchical levels for animals: regnum, classis, ordo, genus, and species. His principal subdivisions of the animal kingdom, that is, the classes, were Mammalia, Aves, Amphibia, Pisces, Insecta (essentially arthropods), and Vermes (essentially everything else). Thus four of the principal animal taxa were vertebrates, and only two classes embraced the entire spectrum of invertebrate animals.

Cuvier (1812) is sometimes credited with erecting a level that corresponds roughly with modern phyla; he called the principal subdivisions of animals embranchements, of which he recognized only four: Vertébrés, Mollusques, Articules (annelids and arthropods), and Zoophytes (echinoderms, cnidarians, and just about everything else). This is a slightly more balanced classification, putting three major invertebrate taxa on equal footing with the vertebrates. Nevertheless, Cuvier's embranchements are clearly on the same level as the classes of Linnaeus. As Cuvier called the subdivisions of the embranchements "classes," it appears that he had defined a higher taxonomic level, but that was not really the case; he simply demoted Linnaeus's term. Cuvier based his embranchements on his perceptions of functional unity within each division (see Appel 1987). Von Baer (1828) found that the same four divisions could be recognized on developmental criteria. The embranchements were used by many eminent naturalists into the second half of the nineteenth century. For example, a classification by Agassiz (1857) used four "branches," and one by Owen (1860) used four "provinces," all essentially the embranchements of Cuvier.

Haeckel (1866) introduced the term phylum, based on the Greek word phylon, a tribe or stock. The phyla were principal subdivisions of the kingdom Animalia, and thus on a level with Linnaeus's classes and Cuvier's embranchements. Haeckel used the term in two ways. In one usage, phyla denoted major branches in his famous trees of life. Six such branches of animals were recognized, although one, Spongiae, was placed in Protista rather than Animalia; the other five were Coelenterata, Echinodermata, Articulata, Mollusca, and Vertebrata. A second usage was as a level in a hierarchical classification. Haeckel (never one to underdo things) used twelve principal categories from species to phylum, each further subdivided by a subcategory, for a total of twenty-four hierarchical levels.

The number of recognized living phyla in hierarchical classifications has grown significantly since Haeckel's time. The classifications used in recent textbooks differ in detail, splitting some phyla and lumping others, but the number of phyla recognized usually lies in the low to middle thirties. Three representative synopses of the animal kingdom employ thirty (Parker 1982), thirty-two (Margulis and Schwartz 1982), and thirty-four phyla (Barnes 1984). Since those synopses were assembled, two additional phyla have been described (Loricifera Kristensen 1983 and Cycliophora Funch and Kristensen 1995), some phyla have been sunk, and a few groups have been raised to phylum rank by some workers.

A century after Linnaeus supplied what became the foundation of zoological nomenclature, Darwin (1859) proposed that the diversity of life had arisen through evolutionary processes, a hypothesis that was thoroughly tested and corroborated in the following century. Organisms are related to one another and can be arranged in a genealogy of life, as humans can be arranged in family trees. Darwin himself produced a treelike diagram of the relations among some hypothetical species (fig. 1.1), and Haeckel (1866) produced a number of trees of life, many complete with bark and gnarled branches (fig. 1.2). Once it was accepted that we owe the diversity of life to evolution, the Linnean hierarchy became a way of expressing relatedness as well as morphological similarity per se. Today it is accepted that each taxon should be monophyletic-that it contains only species that have a common ancestor that is the founding member of that taxon (fig. 1.3). Despite the acceptance of a tree of life, systematists continued to employ the Linnean hierarchy. Until the second half of the twentieth century, phyla were nearly always regarded as composing a hierarchical rank that represented a principal subdivision of the animal kingdom, whether or not they were represented in a tree.

In phylogenetic trees the position of a species (or of another taxon) depends upon its ancestors and descendants rather than its morphology per se. The branches of the tree represent actual entities, and (if the tree is correct) they have historical reality as lineages. The landmarks that are most easily identified in a tree structure are the branch points or nodes. As the nodes in a phylogenetic tree usually represent the onset of independent evolutionary paths for organisms along each branch, systematists often use nodes as the basis for their taxonomic nomenclature (node-based taxa). Identifying the nodes and determining their sequences, or identifying discrete branches in some other way, produces a classification with a treelike structure rather than a hierarchical one. The methodology in common use for determining such a treelike structure was founded by Hennig (1950, 1966), and is termed cladistics.

A branching creates two (or more) sister species; each sister founds a monophyletic taxon-a branch that includes the sister and all descendant branchings, which form a clade. Branches of a phylogenetic tree that include all descendants of a founding species are termed holophyletic (fig. 1.3A); they are also monophyletic, of course. In Linnean taxonomy, monophyletic branches may be divided into several taxa of equivalent rank if they form distinctive morphological clusters. Thus the founding species of a branch, and its cluster, may form a taxon that does not include all of the species descending from it-the taxon is not holophyletic. Such a taxon is termed paraphyletic and can be termed a paraclade (fig. 1.3B; as defined by Raup [1985], the term paraclade included holophyletic clades; Wagner [1999] used it for strictly paraphyletic clades, and that is how it is used here). Such a taxon is also monophyletic since all of its members are descended from its founding species. In Hennigian classifications paraphyletic taxa are not permitted, and thus all monophyletic clades must be holophyletic, which becomes a redundant term. In Linnean classifications a monophyletic clade may be either paraphyletic or holophyletic, so the distinction is not redundant. With either classification system mistakes are sometimes made, and species or other taxa may be included within a higher taxon or clade with which they do not in fact share a founding common ancestor. Groups resulting from such erroneous placements are termed polyphyletic (fig. 1.3C) and should be emended whenever such an error is detected.

The Concept of Homology Is Basic to Determining Animal Relationships

A major source of phylogenetic error lies in confusing homologues with analogues. In evolutionary terms, homologues are similar features in separate organisms or taxa that have evolved from a similar ancestral feature, and owe their similarity to this common inheritance-dog and lizard forelimbs, for example. Analogues are similar features in separate organisms or taxa that have not evolved from a common ancestral feature, that have evolved independently, but that share a common or similar function-bird and bat wings, for example. The distinction between homology and analogy was first developed in preevolutionary times, when homologues were commonly represented as reflections of the characters in some "ideal" type (see Appel 1987). It was Owen (1843, glossary) who originated this usage of the terms homologue and analogue; for him a homologue was "the same organ in different animals under every variety of form and function." Good treatments of homology are in Wiley 1981; Patterson 1988; and papers in Hall 1994 and Bock and Cardew 1999. Morphological features used as criteria of relatedness must have a common evolutionary origin-must be homologous-whether one is constructing a Linnean or a Hennigian classification. Classing birds and bees together because they both have wings is clearly not appropriate. If there were a way to identify morphological homologies unambiguously, it would be much easier to construct an accurate tree of life. Recognition of homologues among phyla has proven difficult. The branching of any two phyla from their last common ancestor has always occurred well before we can identify the phyla morphologically, by which time homologous features have usually diverged significantly. Furthermore, features that have evolved independently for similar functions commonly resemble each other and have often been mistaken for homologues.

The most uncomplicated case of homology, sometimes termed static homology, occurs when a feature is inherited in sister lineages and has remained recognizably similar during subsequent divergence. A complication arises if the feature undergoes significant change during the divergence to create a transformational homology; the feature is then recognized as a distinct character in the transformed lineage (see Streidter and Northcutt 1991). If the transformed characters can be connected by intermediates, they may still fall under the definition of homology, but when the features cease to resemble each other, the concept loses much of its utility. When similar features are repeated serially within the same organism, as with the segments of an earthworm, they are sometimes regarded as serial homologues. In evolutionary terms this usage would imply that they have descended by multiplication of a single ancestral feature, but the history of serial homologues is usually not understood. In many cases so-called serial homologues tend to diverge in time, becoming morphologically and functionally specialized according to their positions along a body to produce a pattern of regionation. Some features exist in multiple similar copies within individuals but not in a serial arrangement, as for example many cell types; such copies are termed homonyms.

Linnean and Hennigian Taxa Have Different Properties

All of the processes that introduce, conserve, and change morphological features are significant components of evolution. Hierarchies and trees are the two structures in which taxa are normally classified, the former in a Linnean system, the latter in a Hennigian one. The hierarchical approach to phyla, as in Linnean classifications, emphasizes patterns of morphological similarity, based on characters that arise and spread among a lineage and its collateral relatives. As a result, a paraclade can be created when a distinctive new morphological group originates from within a taxon and is ranked equally with its parent group. The cladistic approach, as in Hennigian classifications, emphasizes descent, and is based on characters that indicate the sequence of their introduction from ancestor to descendant. As a result, only true clades that include all descendants of the clade ancestor are recognized as taxa. Using a tree or a hierarchy is not simply a choice among different methods of assorting taxa, however, for when treated in these different systems, taxa, including phyla, are defined differently. Each of these approaches provides a distinctive perspective on the phyla and on their roles in the history of life, and to ignore either is to risk missing some of the more basic features of evolution. Understanding the differences in the properties of trees and ranked hierarchies is therefore essential in evaluating the natural relations within and among phyla.

In fact, hierarchy and tree structures occur in most of the biological systems that are involved in the origin and evolution of phyla. Evidently all natural hierarchies are formed by treelike processes. For example, take a metazoan body. Cells proliferate from an egg by subdivision and then duplication, and if the ancestral-descendant relations among cells are traced, they form a treelike branching system. The resulting body is not organized as a tree, however, but as a hierarchy of cells, tissues, organs, and so forth. Another example is the hierarchy of ecological entities forming the planetary biota, from individuals to populations to communities to regional faunas to provinces and realms. The biota is produced by a tree-the tree of life. Furthermore, trees and hierarchies are both found within metazoan genomes (chap. 3), the former producing the latter. And finally, the Linnean hierarchy is clearly formed by a treelike branching process that can be described in Hennigian terms. Before coming to grips with the evolution of these entities, it is most useful to discuss the distinctive properties of hierarchies and trees, indispensable to understanding the way in which the biological world is organized.

Genealogical Histories Can Be Traced in Trees, Which Are Positional Structures

The various family trees, trees of life, and other branching diagrams used in the biological sciences include structures that have often been termed hierarchical, but that do not have the properties of hierarchies (see below). They have other properties, however, that hierarchies do not possess. Trees usually proceed from a single founding unit or "root," tracing the courses of lineages through time; they can order entities in ancestor-descendant relationships. The entities in trees may be clearly individuated, as people in a family tree, or they may grade into each other, as do evolving populations. Gradational lineages can be delineated by one or more criteria, such as, in evolving lineages, by using branch nodes, or periods of rapid morphological change, or the first appearance of some particular feature, or gaps in the fossil record, to define taxonomic entities within the continua. The entities in a tree are all alike-in a family tree, they are all people-while in a hierarchy they are nested into new entities from rank to rank (see below).

Three sorts of positional structure are shown in fig. 1.4. One type contains tiers (fig. 1.4A). This type is exemplified by family trees that are positioned by generations, as discussed above. A second sort of positional structure is exemplified by a series of entities that can be placed in a series, one ahead of another (fig. 1.4B). A single lineage of ancestral to descendant fossil populations would form an example. This structure is analogous to a tree that lacks branches. A third positional structure has branches, but the relations between entities on separate branches are indeterminate (fig. 1.4C). This is the way that taxa are generally positioned within the tree of life.

(Continues...)



Excerpted from ON THE ORIGIN OF PHYLA by JAMES W. VALENTINE Copyright © 2004 by The University of Chicago. Excerpted by permission.
All rights reserved. No part of this excerpt may be reproduced or reprinted without permission in writing from the publisher.
Excerpts are provided by Dial-A-Book Inc. solely for the personal use of visitors to this web site.

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Table of Contents


Preface
Part One- Evidence of the Origins of Metazoan Phyla
1. The Nature of Phyla
Phyla Are Morphologically Based Branches of the Tree of Life
Concepts of Animal Phyla Have Developed over Hundreds of Years
The Concept of Homology Is Basic to Determining Animal Relationships
Linnean and Hennigian Taxa Have Different Properties
Genealogical Histories Can Be Traced in Trees, Which Are Positional Structures
Morphological Entities within Metazoan Bodies, Such as Cells, Can Be Positioned in Trees
Trees Composed of Individual Organisms Can Be Incredibly Complicated
Trees Composed of Species Are Much Simpler
Trees Can Be Formed of Linnean Taxa above the Species Level
Molecular Information Can Position Morphologically Based Taxa in a Tree
Natural Biological Hierarchies Are Nested Structures of Functional Entities That
Emerge When Complex Systems Are Organized
There Are Four Major Types of Hierarchical Structure
Hierarchies Help Sort Out Relations among Biological Features
Novel Phenomena Emerge at Successive Hierarchical Levels
• The Effects of Levels upon One Another Are Quite Asymmetrical
Natural Hierarchies Are Formed by Trees
An Ecological Hierarchy of Biotic Entities Is Formed by the Tree of Life
Hierarchies of Genes Can Be Mapped onto the Somatic and Ecological Hierarchies
The Linnean Hierarchy Is Quasi-Natural
Trees and Hierarchies Have Very Distinct Properties
Cladistics Is a Systematics Based on Trees
Some Cladistic Terms Are Hypotheses as to the Evolutionary Status of Characters
In Cladistic Classifications, Branch Points May Define Sister Taxa That Are Holophyletic
Phyla Have Split Personalities
Molecular Branchings Can Define Clades, while Morphological Features Define Linnean Taxa
Bodyplans Consist of Evolutionarily Disparate Features
Bodyplans Are Polythetic
Important Bodyplan Features May Be Plesiomorphies or Synapomorphies, and May Be Homoplasies
Systematic Hierarchies and Trees: A Summary
2. Design Elements in the Bodyplans of Phyla
Cells Are the Basic Building Blocks of Metazoan Bodies
Cytoskeletons Provide the Framework for Cytoarchitectures
Metazoan Cells Have Descended from Protistans, Probably Choanoflagellate-Like
Cells Are Integrated into Tissues by Protein Bindings or Matrices
Extracellular Matrix Supports Metazoan Tissues
In Most Metazoan Tissues, Cells Are Connected or Anchored by Protein Molecules
Metazoans Have Several Major Types of Tissues
Most Tissues Are Epithelial or Connective
Muscle Tissue May Be either Epithelial or Connective
Nervous Tissues Are Not Organized either as Epithelia or as Connective Tissues
Multinucleate (Syncytial) Tissues Are Found in Many Disparate Phyla
Organs and Organ Systems Are Formed of Tissues
Organisms Are Best Understood as Developmental Systems
Cleavage and Cell Differentiation Are Linked in Most Metazoan Ontogenies
Gastrulation Gives Rise to Ectodermal and Endodermal Germ Layers
Middle Body Layers Range from Simple Sheets of Extracellular Matrix to
Mesodermal Germ Layers
Pseudocoels and Hemocoels Are Body Cavities That Lie on the Site of the Blastocoel
Coeloms Are Body Cavities That Lie within Mesoderm
Some Coeloms Function as Hydrostatic Skeletons
• Some Coeloms Are Adjuncts to Organs
Larval Stages Commonly Possess Bodyplans of Their Own
Many Bodyplan Features Reflect Locomotory Techniques
In Soft-Bodied Forms, Locomotory Devices Range from Cilia to Limbs
"Hard" Skeletons May Complement or Replace the Biomechanical Functions of Fluid Skeletons
Symmetry and Seriation Are the Principal Descriptors of Body Style
Symmetry Is Imparted by Repetition of Parts across Planes or along Radii
Anteroposterior Regionation Involves Seriation, Segmentation, and Tagmosis
Evolutionary Changes in Body Size Occur throughout Metazoan History
Area/Volume Ratios Are Sensitive to Most Size Changes
Life Is Different at High versus Low Reynolds Numbers
Morphological Complexity Is Not a Simple Topic
3. Development and Bodyplans
The Evolution of Developmental Systems Underpins the Evolution of Bodyplans The English Language and Genomes Both Have Combinatorial, Hierarchical Structures
In Narrative English the Immensity of Combinations Inherent in the Alphabet Is Constrained within a Hierarchy
Hierarchical Constraints Also Operate within Metazoan Genomes
The Metazoan Gene Is a Complex of Regulatory, Transcribed, and Translated Parts
Transcribed Gene Regions Are Processed to Produce mRNA
Cis-Regulatory Elements Mediate Transcription
Regulatory Signals Are Produced by Trans-Regulatory Systems
Transcription Factors Bind to Enhancers
Trans-Regulators Are Controlled by Signals That Ultimately Arise from Other Regulatory Genes
Genomic Complexity Is a Function of Gene Numbers and Interactions
Metazoan Genomes Display Surprising Patterns of Similarities and Differences among Taxa
Some Functional Classes of Genes Are Broadly Similar across Metazoan Phyla
Bodyplans Are Patterned by Sequential Expressions of High-Level Regulatory Genes
Anteroposterior Axis Specification and Patterning Genes Are Found throughout Eumetazoa
Dorsoventral Axis Specification and Patterning Genes Are Similar across Bilateria
Organogenesis Involves Positioning by Patterning Genes and Development via Gene Cascades Controlled by Selector Genes
Signaling Pathways, Like Individual Genes, Are Recruited for a Variety of Tasks
Developmental Genomes May Evolve on Many, Semidecomposable Levels
Evolution of Cis-Regulatory Elements Entails Effects That Differ from the Evolution of Transcribed Genes
Regulatory Variation May Be Maintained by Several Unique Mechanisms
Units of Selection in Developmental Evolution Include Semi-independent Modules
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