Evolutionary Patterns: Growth, Form, and Tempo in the Fossil Record

by Jeremy B. C. Jackson, Scott Lidgard, Frank K. McKinney

Overview

With all the recent advances in molecular and evolutionary biology, one could almost wonder why we need the fossil record. Molecular sequence data can resolve taxonomic relationships, experiments with fruit flies demonstrate evolution and development in real time, and field studies of Galapagos finches have provided the strongest evidence for natural selection ever measured in the wild. What, then, can fossils teach us that living organisms cannot?

Evolutionary Patterns demonstrates the rich variety of clues to evolution that can be gleaned from the fossil record. Chief among these are the major trends and anomalies in species development revealed only by "deep time," such as periodic mass extinctions and species that remain unchanged in form for millions of years. Contributors explore modes of development, the tempo of speciation and extinction, and macroevolutionary patterns and trends. The result is an important contribution to paleobiology and evolutionary biology, and a spirited defense of the fossil record as a crucial tool for understanding evolution and development.

The contributors are Ann F. Budd, Efstathia Bura, Leo W. Buss, Mike Foote, Jörn Geister, Stephen Jay Gould, Eckart Hâkansson, Jean-Georges Harmelin, Lee-Ann C. Hayek, Jeremy B. C. Jackson, Kenneth G. Johnson, Nancy Knowlton, Scott Lidgard, Frank K. McKinney, Daniel W. McShea, Ross H. Nehm, Beth Okamura, John M. Pandolfi, Paul D. Taylor, and Erik Thomsen.

Product Details

ISBN-13:	9780226389318
Publisher:	University of Chicago Press
Publication date:	08/01/2001
Edition description:	1
Pages:	344
Product dimensions:	6.00(w) x 9.00(h) x 1.00(d)

About the Author

Jeremy B. C. Jackson is director of the Center for Tropical Paleoecology and Archeology at the Smithsonian Tropical Research Institute and the William and Mary B. Ritter Professor of Oceanography at the Scripps Institution of Oceanography.

Scott Lidgard is an associate curator of fossil invertebrates in the Department of Geology at the Field Museum, lecturer in the Committee on Evolutionary Biology at the University of Chicago, and adjunct associate professor of biology at the University of Illinois, Chicago.

Frank K. McKinney is a professor emeritus in the Department of Geology at Appalachian State University and Honorary Research Fellow in the Department of Palaeontology at The Natural History Museum, London.

Read an Excerpt

Evolutionary Patterns: Growth, Form, and Tempo in the Fossil Record in Honor of Allan Cheetham

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By Frank K. McKinney

University of Chicago Press

Copyright © 2001 Frank K. McKinney
All right reserved.
ISBN: 0226389316

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Growth by Intussusception in Hydractiniid Hydroids

Leo W. Buss

Forms that appear complex to the human eye can be generated by the iterative application of a small number of global rules (Ulam 1962, 1966). A large literature has developed in which rules are chosen and the morphology of plants, fungi, and colonial invertebrates mimicked (e.g., Braverman and Schrandt 1966; Leopold 1971; Cheetham et al. 1980; Waller and Steingraeber 1985; Bell 1986; Kaandorp 1994). The correspondence of simulations to actual organisms is sufficiently faithful that such techniques are often the tools of choice for representations of organisms in computer graphics (Prusinkiewicz and Lindenmayer 1990). I am aware, however, of no study that establishes any such rule in any living organism.

The rule schemata that generate such faithful computer images are often of this sort: "inspect the grid, identify all stolons that have grown by four units, place a branch at midpoint of new growth," "inspect the grid, identify all locations where three or more stolons have anastomosed, place a polyp at each such location," and so on. These are instructions for a computer; no sessile invertebrate possesses thecapacity to assess its state and update development in this way.

Or do they? Clonal organisms typically possess one or more clonewide fluid-conducting systems (e.g., the phloem system of vascular plants, the system of cytoplasmic streaming within the hyphae of a fungal mycelium or the plasmodium of a myxomycete, the gastrovascular system of cnidarians, and the blood vascular system of certain colonial ascidians). The functioning of these systems will generate local patterns of pressure distribution, shear stress, and surface tension experienced by the tissues, cells, and/or membranes lining the conducting system. If such features can be detected and the signals transduced to effect expression of pattern-forming genes, global rules responsive to local state arise.

I will explore the suggestion that hydroid colony form arises from such a process of self-inspection. All hydroids share one colonywide physiological conducting system, the gastrovascular system. If the functioning of the gastrovascular system generates local hydrodynamic signals which, in turn, trigger specific morphogenetic pathways, then perturbations of gastrovascular circulation should have marked effects on colony morphology. I review evidence that this is the case. Hydroid colony form largely derives from patterns of stolon branching and placement of polyp buds atop existing stolons. If colonies self-inspect, features of gastrovascular circulation may trigger one or both of these events. I suggest specific biophysical features that may govern polyp placement and stolon branching and provide new observations, collected in the honor of Alan Cheetham, in support of one such suggestion. Finally, a model of growth by intussusception implies that colony-patterning genes exist, specifically those associated with the placement of polyps and the branching of stolons, and that their expression is regulated in accord with hypothesized biophysical signals. I review the progress toward identifying such genes.



Manipulation of Gastrovascular Circulation Alters Colony Form

Gastrovascular circulation and colony morphology are inevitably linked. Colony morphology is the disposition in space of a system of pumps (i.e., polyps) coupled to one another by a system of pipes (i.e., stolons). Changes in the relative sizes or spatial distribution of pumps and pipes will, as a matter of mechanical necessity, modify the pattern of circulation of fluids contained within them. What is at issue is whether such changes are a two-way street. Specifically, do changes in circulation elicit subsequent changes in the morphology? Experiments to this end have been performed in Podocoryna carnea (Sars 1846) and Hydractinia symbiolongicarpus (Buss and Yund 1989).

Podocoryna carnea is an athecate hydrozoan of the family Hydractiniidae, which develops a typical filiform colony (fig. 1.1). The colony is composed of feeding polyps connected to one another by stolons, which adhere to the substratum. Colonies grow by the elongation of stolon tips, the branching and anastomosis of tips (which establish and eliminate growth zones, respectively), and the placement of polyps atop existing stolons.

The gastrovascular system of Podocoryna, like that of all colonial hydroids, comprises the digestive lumens of the polyps together with the lumens of the stolons which couple polyps to one another. Fluid within this lumen is circulated to effect colonywide gas exchange and nutrient distribution. Muscles and nerves are limited to the polyps (Stokes 1974; Schierwater et al. 1992). Hence, exclusive of epithelial conductance, the gastrovascular system is the sole colonywide conducting system in this species.

Circulation of hydroplasm is effected by the periodic contraction of muscles in the polyps, which drives fluid from the digestive cavity of the polyp into the lumen of stolons (fig. 1.2), which, in turn, expand to accommodate the increased volume (Wagner et al. 1998; Dudgeon et al. 1999). Gastrovascular circulation is easily monitored in the peripheral stolons of a colony. Fluid flows into the blind tip of a stolon until the stolon is maximally distended, at which point the direction of flow is reversed and fluid flows away from the tip, collapsing the internal lumen (see, e.g., Wyttenbach 1973; Buss and Vaisnys 1993; Van Winkle and Blackstone 1997). Flow within stolons, thus, is sequentially bidirectional, and for peripheral stolons, the volume flux per cycle is proportional to the diameter of the stolon (Van Winkle and Blackstone 1997).

To assess whether perturbation of gastrovascular physiology induces alterations in subsequent colony morphology, a series of experiments has been performed wherein a colony was exposed to 2,4-dinitrophenol (DNP), gastrovascular flow assayed at stolon tips, and subsequent development monitored (Blackstone and Buss 1992, 1993; Blackstone 1997, 1998b). DNP is an uncoupler of oxidative phosphorylation; hence, application of DNP reduces the amount of ATP available to a colony. Since the circulation of fluids within a colony is an active metabolic process, requiring muscular contraction, one might expect that application of DNP would disrupt gastrovascular circulation. This proved to be the case. Figure 1.3 shows the expansion and contraction cycles of a peripheral stolon of control and DNP-treated colonies. After 3 days of treatment with 1 µM DNP, the amplitude of stolonal expansion, and hence volume flux to the tip, is markedly depressed (fig. 1.3A). After 5 days of DNP treatment, stolonal oscillations have been effectively eliminated (fig. 1.3B).

The effect of DNP treatment on subsequent colony development was pronounced. DNP treatment increased the rate of stolonal branching and the rate of polyp bud formation (e.g. 1.4). The relationship is that which one might expect. When the energy available to pump the fluid is decreased, the pipe must either be shortened or the number of pumps increased to maintain a given volume flux to the end of a pipe. Branching achieves the former, bud initiation the latter. Indeed, the colonies appear to be seeking to maintain a given volume flux to the tips; after 3 weeks of morphological response to DNP treatment, stolonal contractions in control and DNP-treated colonies display near-identical amplitudes (fig. 1.3C).

The DNP experiments demonstrate that perturbations to gastrovascular circulation induce two pattern-forming systems: stolonal branching and bud initiation. DNP treatments transform relatively "runnerlike" colonies (sensu Buss 1979; Jackson 1979), characterized by longer stolons, fewer branches, and fewer polyps per unit stolon length into a "sheetlike" colony, characterized by shorter stolons, more branches, and more polyps per unit stolon length.

In these experiments, colonies of identical morphology were shown to develop differently if gastrovascular circulation was perturbed. Alternatively, one might ask whether colonies selected for differences in their morphology display corresponding differences in patterns of gastrovascular circulation. Blackstone (1998a) mated field-collected colonies of Podocoryna and established two genetic lines from the F1. He brother-sister inbred both lines and, in each generation, selected for sheetlike morphologies in one line and runnerlike morphologies in the other. After six generations of inbreeding, he assayed flow to the stolonal tip. As expected on the basis of the DNP experiments, the line inbred for sheetlike morphologies displayed significantly lower volume fluxes to peripheral stolons than that of the line inbred for runnerlike morphologies.

The influence of colony morphology on patterns of gastrovascular circulation is particularly clearly illustrated in another hydractiniid hydroid, Hydractinia symbiolongicarpus. Hydractinia colonies differ from those of Podocoryna in one prominent feature. Early in colony ontogeny, the basal ectoderm of the body column of the polyp expands from the polyp base and overtops the stolonal nexus (Cartwright and Buss 1999). This tissue, the stolonal mat, expands peripherally as a sheet. Stolons within the mat are arranged as both radial and circumferential, or ring, canals (fig. 1.5A). Radial canals may or may not extend beyond the mat periphery as free stolons, and ring canals may or may not be continuous along the mat periphery (fig. 1.6A).

Dudgeon and Buss (1996) show that sheetlike Hydractinia colonies, that is, those with small ratios of free stolon length to stolonal mat area, display little variation in radial canal diameter, wider ring canal diameter, and higher frequencies of continuous ring canals than do runnerlike colonies (see Dudgeon and Buss 1996, tables 1 and 2). The greater disparity in stolon radii in runnerlike forms derives, in large measure, from the presence of free stolons in runnerlike forms, which bear larger radii and which frequently disrupt the continuity of ring canals.

Differences in radii of stolons is of considerable physical significance. The volume flux for flow through a pipe for the low Reynold's number, laminar flow regimes relevant here is approximated by Hagen-Poiseuille law, wherein volume flux is proportional to the fourth power of radius (see, e.g., Fung 1993). Thus, for a given pressure head and stolon length, the larger peripheral stolons of runnerlike forms will experience vastly greater volume fluxes to their tips than will the smaller radial canals within the stolonal mat (fig. 1.6B). If growth rate is proportional to volume flux, then free peripheral stolons may be expected to elongate at relatively faster rates. The pattern of gastrovascular circulation that is induced by the morphology of a runnerlike form may be expected, then, to generate faster growth of peripheral stolons than mat tissue, that is, to create the very conditions necessary to maintain a runnerlike form.

A converse argument applies to sheetlike colonies. Here the periphery is characterized by a wide circumferential ring canal into which smaller radial canals enter and out of which comparable-sized extensions of the radials exit (fig. 1.5B). Since all tips are of comparable size and all draw fluid from the same wide-bore ring canal, they may be expected to experience comparable volume fluxes and, hence, to elongate at comparable rates. Equal circumferential growth rates result in sheetlike morphologies, just as unequal growth rates between free stolons and stolonal mat generate runnerlike forms.



Continues...

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Excerpted from Evolutionary Patterns: Growth, Form, and Tempo in the Fossil Record in Honor of Allan Cheetham by Frank K. McKinney Copyright © 2001 by Frank K. McKinney. Excerpted by permission.
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Table of Contents

Preface

Part 1. Modes of Development, Hierarchies of Morphological
Organization, and the Adaptive Significance of Colony Form
1 Growth by Intussusception in Hydractiniid Hydroids
2 Parts and Integration: Consequences of Hierarchy
3 Refuges Revisited: Enemies versus Flow and Feeding as
Determinants of Sessile Animal Distribution and Form

Part 2.Recognition of Species, and the Tempo of
Speciation and Extinction
4 Recognizing Coral Species Present and Past
5 Geologically Sudden Extinction of Two Widespread
Late Pleistocene Caribbean Reef Corals
6 Linking Macroevolutionary Pattern and
Developmental Process in Marginellid Gastropods
7 The Interrelationship of Speciation and
Punctuated Equilibrium

Part 3.Macroevolutionary Patterns and Trends
8 On the Ends of the Taxon Range Problem
9 Evolutionary Rates and the Age Distribution of
Living and Extinct Taxa
10 Contrasting Patterns in Rare and Abundant Species
during Evolutionary Turnover
11 Asexual Propagation in Cheilostome Bryozoa:
Evolutionary Trends in a Major Groups of
Colonial Animals
12 Macroevolutionary Trends: Perception Depends on
the Measure Used

List of Contributors
Index

Editorial Reviews

Geologists, biologists, oceanographers, and other scientists from the U.S., Europe, and Panama, describe the information available from the fossil record and its implications for our understanding of evolution. In these twelve essays, they discuss the modes of development, species recognition, the rhythm of speciation and extinction, and macro- evolutionary patterns and trends. Many of the papers were presented at a 1997 conference in Salt Lake City, Utah. Annotation c. Book News, Inc., Portland, OR (booknews.com)

Booknews