body plan.pdf

Riedls Burden and the Body Plan: Selection,Constraint, and Deep Time

RAINER R. SCHOCH

Staatliches Museum fur Naturkunde, Rosenstein 1, Stuttgart, Germany

ABSTRACT Rupert Riedls concept of burden forms a causal hypothesis on organismicintegration and evolutionary constraints. Defined as the hierarchically nested interdependence ofcharacters within the organism, burden was seen as (1) defining and conserving body plans and (2)constraining and directing evolutionary trajectories. A review of the components of the burden conceptreveals important consistencies with the modern tenets of evo-devo. This concept differs from thecurrent consensus of evolutionary theory in that it (1) grants evolution less options for changingtightly integrated, locked-in characters and (2) in deducing from this an ever decreasing freedom forevolution, with cyclism and typostrophism as resulting macroevolutionary phenomena. Despite thesedifferences, I show that the burden concept was consistent with most major tenets of the ModernSynthesis, and Riedl attempted to explain patterns of large-scale evolutionary trends exclusively bymicroevolutionary (gradualistic) processes. The burden concept is fruitful and unique in its focus onhierarchically nested constraints and resembles the hierarchical architecture of gene regulatorynetworks. However, such networks are more high-dimensional and most of their components appearto be easier to evolve than Riedls burden. Yet in combination with evolvability, a modified concept ofburden might contribute substantially to the understanding of organismic integration and the long-term evolution of body plans. J. Exp. Zool. (Mol. Dev. Evol.) 312B, 2009. r 2009 Wiley-Liss, Inc..

How to cite this article: Schoch RR. 2009. Riedls burden and the body plan: selection,constraint, and deep time. J. Exp. Zool. (Mol. Dev. Evol.) 312B:[page range].

The relationship between the study of macro-evolution, developmental biology, and the Syn-thetic Theory of Evolution is currently in a stateof major revision and controversy. After decades ofparallel development and conceptional separation,these fields are now becoming increasingly inte-grated, with divergent approaches and opinions ontheir mutual relationship emerging at a fast pace(Raff, 96; Hall, 96, 99; West-Eberhard, 2003;Pigliucci and Kaplan, 2006). The reasons for thisnovel interest in a field that had long beenconceived to be trapped with mines and pitfallsare at least twofold: (1) developmental biology hasmade tremendous advances in elucidating thegenetic and regulatory causation of morphogenesis,and (2) in the last decades, broad-scale cladisticanalyses integrating extant and fossil taxa havebeen carried out for many larger groups oforganisms, revealing large-scale patterns of phylo-geny. These developments have paved the way for afundamental re-evaluation of macroevolution.

The study of macroevolution is defined hereas the analysis of processes that generate the

phylogenetic patterns apparent at the levels ofspecies and clades. It does not imply here that theseprocesses are necessarily different from those ofmicroevolution, contra the practice and conceptionof some authors (e.g., Stanley, 79; Gould, 2002), orthat macroevolution involves multi-level selectionand sorting. Ever since Darwin (1859), the majorquestion has been whether macroevolutionaryprocesses can be completely reduced to the causesoperating at the level of the population, or whetherthere are additional factors involved, such asselection among species and clades, or proximatefactors within the organism.

During the 55-year period between Darwins death(1882) and the advent of the Modern Synthesis(1937), the domain of macroevolution gained

Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/jez.b.21300

Received 27 February 2009; Revised 4 May 2009; Accepted 12 May2009

Correspondence to: Rainer R. Schoch, Staatliches Museum furNaturkunde, Rosenstein 1, D-70191 Stuttgart, Germany. E-mail:[email protected]

r 2009 WILEY-LISS, INC.

JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 312B (2009)

increasing interest and was approached from atleast two different perspectives: (1) geneticists likeBateson (1894), de Vries (01) and Goldschmidt(27, 40) envisioned large-scale mutations to havean impact on the origin of new species and wholeclades, and (2) paleontologists such as Osborn (1893),Dollo (1893), Cope (1870), Beurlen (26), Abel (29),and Schindewolf (36) reported large-scale patternsderived from the fossil record, which they inter-preted as directed trends in evolution. The tenetsof both these fields (schools) embraced unortho-dox components not readily in agreement withDarwinism and the Modern Synthesis (see below).In this alternative, most of phylogeny was referredto processes different from those suggested byDarwin. This antithesis to the Modern Synthesisformed the starting point for subsequent authorslike Rupert Riedl and Stephen Jay Gould whosought to synthesize the divergent views on micro-and macroevolution.

The present review is focused at the relationshipbetween mechanisms of development, naturalselection, and the patterns of macroevolution,and it begins with the perspective of Riedl(77, 78) on this topic. Riedls approach isparticularly apt as a starting point, because hewas quite unique among morphologists in restrict-ing the causes of macroevolution to developmentalmechanisms and selection, and by accepting theModern Synthesis as the main framework forevolutionary studies. However, despite his generalacceptance of this framework, Riedl regarded thesynthesis as incomplete: in his view, it fell shortin explaining two general patterns of order inorganisms, (1) the static pattern of the body plan(Unity of Type in Darwins terminology), and (2)the dynamic pattern of directed trends in large-scale phylogeny (Riedl, 77). At that time, both ofthese patterns had been pushed aside or wereviewed with great suspicion. Riedls view on theincompleteness of the Modern Synthesis, thenclose to heresy, is now much highlighted and putforward by a range of present authors (e.g., Raff,96; Arthur, 97, 2004; West-Eberhard, 2003;Davidson and Erwin, 2006). While the body planproblem has emerged as one of the main centers ofresearch in evo-devo, orthogenesis became a dirtyword, and from the perspective of causality quiterightly so, because proponents of the concepteither failed to offer causal explanations at all orreturned to prescientific ideas of vitalism (Reif,86; Futuyma, 2006). Yet in Riedls view, body planand directed trends were consequences of thesame causal mechanisms, and one of his most

eminent ideas was the concept of burden, whichforms the focus of this review.

A reanalysis of Riedls burden concept isprompted by (1) the success of developmentalevolution or evo-devo in explaining mechanisms ofdevelopment and their role in the establishment ofbody plans, and (2) the results from almost threedecades of cladistic analysis in numerous groups oforganisms (leading to the recognition of large-scale patterns in the fossil record).

RUPERT RIEDLS CONCEPT OF BURDEN

By his focus on causal explanation rather thanterminological book-keeping, Riedl differs frommost previous authors. In contrast to these, herejected idealistic and vitalistic ideas but reliedexclusively on then-known mechanisms of embry-onic induction and physiological functions; he didnot postulate any additional principle or causalfactor outside the ones known to biologists. Further,in stark contrast to another major proponent ofa strictly causal explanation of macroevolution,Goldschmidt (27, 40), Riedl did not embracesaltationism. Instead, he was a staunch proponentof gradualism and the unspectacular, incrementalorigin of clades and their defining characters. Inother words, for Riedl (78), the major differencesbetween phyla started by small changes of char-acters. In this respect, as in most others, Riedlsideas were entirely consistent with the ModernSynthesis, which was stressed by Ernst Mayr in1975, when writing a letter to Riedl referring to thefirst publication of his book in German (Riedl, 2003).

However, Riedl (77, 78) shares with someaforementioned authors the acceptance of cyclism,a traditional concept first fully formulated byHaeckel (1866), meaning a causal parallelismbetween ontogeny and phylogeny. Cyclism wasone reason why Riedl had to deal with the anti-Darwinian theory of typostrophes, despite its firmfoundation on saltationism and the grave contra-dictions with the Modern Synthesis. It is probable,although it has not been explicitly written, thatRiedls views were not appreciated in the way theyshould have by his colleagues because of hisadoption of some of these concepts.

Riedls approach was passionately focused onmorphology, partly because at that time the causallinks between morphology and the genetic back-ground of development were entirely unknown.The more important reason for Riedls focus washis belief in what he termed a causal morpho-logy required to bridge the gap between ultimate

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J. Exp. Zool. (Mol. Dev. Evol.)

(adaptationist) explanations of biological form andthe proximate genetic/epigenetic mechanisms thatgenerate biological structures in the first place.Although Riedl employed some very problematic,early 20th century concepts of macroevolution (seebelow), I shall argue that his ideas on the origin andnature of constraints were consistent with currentevolutionary theory (Wagner and Laubichler, 2004;Budd, 2006). However, he may be unique in combin-ing major tenets of the Modern Synthesis with thoseof orthogenetic macroevolutionary theories. As Riedl(78) put it himself, he was keen to form a balancebetween these two views, both of which he argued tobear fundamental truth despite the various contra-dictions. This may be explained by his strong belief ininterdisciplinary approach in science, which wasinfluenced by his Viennese biography (Wagner andLaubichler, 2004). In addition, Riedl believed theSynthetic Theory to be essentially incomplete in thatit failed to deduce macroevolutionary patterns fromthe theory of population genetics. This triggered hissearch for systemic properties regulating and direct-ing evolutionary change in addition, not in contrast toselection.

Burden: The cause of lawful order

In his book Order in Living Organisms, Riedl(78) developed the concept of evolutionary burden.It forms a keystone in his theory on the origin oforganismic order, set out to explain the hierar-chical structure of body plans and large-scalepatterns of macroevolution. Burden was one ofRiedls solutions to the problem of how order wasmaintained in organisms: the likelihood that acharacter changes during evolution depends on thenumber and importance of functions and charactersdepending on it (Wagner and Laubichler, 2004). InRiedls view, the origin of characters could beexplained in mechanistic terms and each characterequaled a function (responsibility). The moredeeply rooted this function was within the causalweb of the inclusive organism, the higher was itsburden and less probable its evolutionary change.Characters of course could lose functions comple-tely during evolution, and then become probablecandidates for reduction and eventual loss, butsuch modification was seen as restricted to charac-ters with low-ranking burden, confined to traitsoccupying more peripheral positions in the hierar-chy of functions.

Riedl (78) highlighted that burdens acted onboth functionalanatomical units and develop-mental-epigenetic systems within the organism.

His starting observation was that characters hadwidely different rates of evolution, with body plancharacters being the most conservative. Riedl thentook a mathematical approach to morphology,calculating the probability (predictability) of orderin organisms. Body plan characters, in this sense,were the most predictable since conservativefeatures. By that line of reasoning, he suggestedthat individual burdens could even be measured.He suggested to quantify burden by application ofinformation theory.

It is a strength of the burden concept that itembraced both embryonic mechanisms (inductionand morphogenesis) and physiological functions.It highlighted the large extent of integration andinterdependence of body parts. Riedl describedbody plans as controlled by both developmentaland functional necessities, and sought to hold abalancing position between structuralism (focusedon developmental, inner-organismal traits) andfunctionalism in the version of the ModernSynthesis (focused on the organismenvironmentrelation). Following Whyte (65), he went beyondthis dialectics in highlighting powerful functionaldemands inside organisms, granting the internalcomponent of selection the predominating role inbody plan evolution. Consequently, burden was adirect measure of the organismal integration of atrait and the selection pressure acting on it.

Although Riedls burden concept was largelytheoretical, he managed to present some convincingand immediately intuitive cases. The most pictorialexample was the hierarchically nested pattern ofarteries in the human arm, visualizing the hierar-chical ranking of burden or responsibility of acharacter. This also formed the starting point forthe attempt to calculate the rank of a functionalburden: the more functions a morphological featurewas controlling, the higher its rank and functionalburden. An analogous hierarchy was proposedfor developmental events and their own hierarchyof burdens, exemplified by the notochord or thebranchial arteries. Riedl argued that both struc-tures were retained in tetrapod embryos, althoughthey were of no functional use in adults; heconcluded that these features possessed a high-ranking epigenetic burden. Thus, an outstandingfeature of Riedls burden concept is its strictemphasis on causality. The main effect of burdenwas that neither development nor function could bechanged isotropically, a pattern that is consistentwith the modern understanding of evolutionaryconstraint (Maynard Smith et al., 85; Schwenk,95; Schwenk and Wagner, 2003).

RIEDLS BURDEN AND THE BODY PLAN 3


Burden and the Modern Synthesis

In two crucial points, the burden concept isconsistent with the Synthetic Theory: (1) itaccepts selection as the major ultimate cause ofevolution and (2) it rejects evolutionarily success-ful macromutations and saltations. In addition tothat, he stressed that constraints on morphologywere to be explained by either developmental orfunctional responsibilities inside the organism.This point was as essential for Riedl as the twoaforementioned, but went beyond then-agreedtenets of the Synthesis. Although organismicintegration was highlighted by others as well(Waddington, 57; Whyte, 65), Riedls approachwas more detailed and complete, and he explicitlyshowed that such internal aspects were not inconflict with selection and gradualism.

Riedl (78) explicitly dismissed Goldschmidtsview on macromutations and argued for smallsteps to be the only effective way for the genome toevolve. As Wagner and Laubichler (2004, p 98) putit, characters do not arise as body plan char-acters. In fact being a body plan character is notan intrinsic property in itself, but rather dependson the way the character is integrated into thenetwork of functional and developmental inter-dependencies in the organism. This point isessential, because despite Riedls occasional refer-ral to patterns employed by saltationist macro-evolutionary theories (e.g., the TypostropheTheory), he clearly adhered to microevolutionand the stepwise acquisition of clade-definingcharacters.

Burden: Inevitable Evolutionary Sclerosis?

The unique feature of the burden concept is theemphasis of hierarchical nesting of multiple bur-dens, which had hardly been studied before. Thiswas derived from one of Riedls four principles oforder, namely the hierarchical structure of allorganisms. Therefore, high-ranking burdens wereregarded (almost) unbreakable, for violations ofburden might unavoidably lead to reduced fitness.Furthermore, the addition of new characters neces-sarily shifted the rank of the existing characters toa higher position, making these characters moreheavily constrained still, while an option for thereverse case was not envisoned. On the contrary,many developmental constraints have been shownto be breakable by recent authors (MaynardSmith et al., 85; Schwenk and Wagner, 2003). Riedl(77) held that the stronger a particular burden was,the less possible its evolutionary change. In its

extreme version, it would result in what may becalled evolutionary sclerosis: old systems, func-tionally essential and highly interconnected, orburdened, will be found to be genetically tightlyinterdependent and in principle unalterable. Riedl(77, p 362) listed such (in his view) extremeburdens, such as the vertebral column, cerebralnerves, vertebrate eye, notochord in chordates, andDNA in organisms. Riedl described the effect ofsuch strong burden as cementation of structures,functions, and pathways beyond and often inopposition to new functional requirements (Riedl,77, p 363, my emphasis). Thus, strong orthogenesiswas a direct consequence of burden for Riedl.

BURDEN IN MODERN VIEW

The burden concept makes a number of pointsthat are worth to be analyzed in the context ofcurrent evolutionary thinking. The two mostgeneral aspects are the origin and maintenance ofbody plans and the directedness of macroevolution.The body plan problem has been much morehighlighted recently, and I shall expand on thistheme by comparing Riedls ideas with recentfindings of gene regulation. In the following Ireview the two major aspects of the burden concept,analyzing their support or the lack of support bythe findings of current evolutionary biology.

Burden, Constraint, and Selection

For Riedl, the single general cause of burden wasselection. This is remarkable, because many otherauthors dealing with the phenomenon of con-straint followed a dichotomous approach in whichconstraint and selection formed opposing factors(e.g., Maynard Smith et al., 85; Arthur, 97).In recent time, this view has been shown to beproblematic (Amundson, 94; Schwenk andWagner, 2004; Brigandt, 2007), because it rulesout that selection may itself cause patternsconsistent with those usually referred to a con-straint, such as evolutionary stasis of a characterdespite being subject to an external selectionpressure for change. In highlighting selection asthe ultimate cause of burden, Riedls position wasmore consistent with the Modern Synthesis thanthe dichotomous approach, which deduces con-straints from mechanisms located at the proxi-mate level (Maynard Smith et al., 85).

Like Whyte (65), Riedl distinguished internalfrom external components of selection, with theinternal component focused at the functionalityof inner-organismal traits and systems. This

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functionality is independent of the actual environ-ment in which an organism lives, and travels withthe organism wherever it goes (Schwenk andWagner, 2001, 2004). Defined as such, the majorfactor of such an internal functionality selectionis stabilizing selection. Similar to sexual selec-tion, internal components of selection maycounter external ones, leading to trade-offs bet-ween organismal and environmental influences(Schwenk and Wagner, 2004). This was the truemeaning of Riedls repeated statement that inter-nal selection could act against external selection.(It is probable that advocates of the ModernSynthesis did not see this point or mistook it forsome anti-Darwinian perspective, whereas inreality this was a more specific and clear-cutdescription of processes leading to body plancharacters, a topic largely neglected by manyevolutionists then.)

Despite essential similarities, Riedls concept ofburden differs from the internal selection conceptof constraint (Schwenk and Wagner, 2003, 2004)in the following aspects.

(1) Riedls burdens were hierarchically structuredand by that formed one of the causes ofhierarchy in organisms. A particular burdenbecame stronger, when new characters wererecruited under its dominance.

(2) The strength of a given burden directly cor-related with its phylogenetic age. As forconstraints, this is not universally so: physicalor chemical constraints do not change withtime, but are present whenever the necessaryboundary conditions are fulfilled. With con-straints maintained by internal selection, thecorrelation of phylogentic age and strength ofburden is also not obligatory.

(3) The evolution of burden was a one-way road; aparticular burden could only grow stronger,except the context in which it was embeddedwas simplified. Budd (2006) has shown thatthis does not hold for constraints and themodern understanding of morphological char-acter evolution.

(4) New burdens were continuously added inevolution, with the implicit effect that thenumber and dominance of burden increasedconstantly within a clade. According to Riedl,this had important effects on macroevolution,namely orthogenesis. The modern concepts ofconstraint are much more cautious withrespect to the deduction of evolutionary trendsin deep time.

Burden and Evolvability

In addition to the burden concept, Riedl putforward another idea that has been much high-lighted recently: evolvability, or the ability ofpopulations to adapt through natural selection.Evolvability increases with the capacity of a genometo produce heritable variation (Wagner, 2008), whichcontrols the extent of raw material for selection toact upon. A basic observation, supported by manyrecent studies, is that genetic complexity does notstrictly correlate with phenotypic complexity. Like-wise, the degree of morphological differentiationbetween related species is not strictly proportional tothe genetic differences between them (Nijhout, 90).Consequently, Riedl suggested that there was apartial mismatch between the organization of thegenotype and that of the phenotype, and it waslogical that internal selection would tend to bridgethis gap. In other words, genome organization(hierarchical gene regulation) would evolve to matchfunctional necessities (hierarchically burdened)within the organism. Riedl (78) therefore suggestedthe metaphor of a genome structure imitating thephenotypes functions (imitatory epigenotype).

The capacity of the genome to evolve in such amanner is a case of evolvability, a concept whichhas become its own dynamic field within evolu-tionary biology (Wagner and Altenberg, 96;Wagner, 2008; Draghi and Wagner, 2009). Oneprobable result of such a concerted genotypephenotype (GP) evolution is the origin of pheno-typically robust morphologiesthe body plans. Atthis point, the positive property of evolvabilityentangles with the (seemingly) negative propertyof burden: the hierarchically regulated genome isforced by selection to increasingly match hierar-chically organized functional demands.

It was only one further step (prepared, but nottaken by Riedl) to visualize body plans as robustplatforms for evolution to act upon. In addition toguaranteeing functional viability, burden alsodefines the frame for evolvability, reducing func-tional redundancy, and deciding which variationsare accessible and which not. As such, body plandefining constraints or burdens may eliminate theadaptively redundant degrees of freedom, thusproviding the necessary robustness for adaptiveevolution to work at all (Wagner and Laubichler,2004). This point is more apparent today than inRiedls time, and it essentially weakens thenegative effect of burden; evolvability grants muchmore freedom to evolution than the originalburden concept envisioned.



Burden and Gene Regulation

The body plan problem has attracted enormousinterest after a surprising match between generegulatory networks (GRNs) and embryonic me-chanisms of body patterning has been elucidated(Raff, 96; Hall, 96; Arthur, 97; Davidson, 2001;Shubin et al., 2009). Finally, the mechanisms thatdefine morphology appear to be in reach ofexperimental investigation (Hall, 2003). In unco-vering these complicated causal relations, it isfurther hoped to understand the origin of givenbody plans, their distinctness, and the processesthat have maintained body plan characters forhundreds of millions of years. In recent years,GRNs have come into focus of that field, after theyturned out to be one of the main levels at whichthese central issues are defined (Davidson andErwin, 2006).

The structure of Riedls hierarchically nestedburdens resembles that of GRNs, although thelatter lie at a much deeper level of organizationthan the cascades of embryonic induction origin-ally employed as an illustration by him. Davidsonand Erwin (2006) showed that the architecture ofGRNs is inherently hierarchical: each phase ofdevelopment has beginnings, middle stages, andprogressively more fine-scale terminal processes,so that network linkages operating earlier havemore pleiotropic effects than those controllingterminal events.

Riedls tenets agree with the findings of Davidsonand Erwin in the following points: (1) differentcharacters (and different GRNs) evolve at greatlydifferent rates, (2) the body plan (and the regula-tory genome) fall into central, intermediate, andperipheral domains, which form a hierarchicallynested pattern of interdependencies, (3) the centraldomains are the most conservative in evolution(bearing the highest responsibilities), while theperipheral regions are the most plastictheyform free ends for selection to act upon. Davidsonand Erwin (2006) termed the central domain thekernel of a GRN. Kernels form subcircuits of generegulation usually consisting of 38 genes, in whicheach gene forms an essential component; mutationwithin kernels is likely to have disastrous effectson the function of the whole network and thus onthe phenotype (Erwin and Davidson, 2009). Askernels often define the fundamental framework ofbody parts, deficient kernels lead to the absence ofthe given anatomical region. The result is a highdegree of evolutionary conservation in kernelarchitecture.

By analogy to hierarchies of functional burdens,Riedl envisioned developmental hierarchies asa continued succession of branching events(5alternative states in development). In contrastto this tree metaphor, the regulatory genome is nowknown to form a network composed of numerousrecursively wired circuits and subcircuits, whichoften cluster around powerful central domains(kernels). The main operations that set up thisregulatory architecture are positive and negativefeedback relations plus the AND processing func-tion, which demands that all inputs are required forthe element to run at a given level (Davidson, 2001).The complicated hierarchy of this built-in logicsrelates directly to developmental processes such asregional specification, pattern formation, cellulardifferentiation, and tissue morphogenesis. That is,mechanisms regulated by kernels are central to thewhole network and therefore most conservative,while details of differentiation and morphogenesisare executed by gene batteries in the peripheraldomains of the GRN, for which numerous muta-tional variants are in reach. In addition to theserather fixed domains of the regulatory hierarchy,there are also more flexible elements called plug-ins.These form regulatory units that may be deployedin various parts of the GRN, and they do not holdfixed positions within the regulatory hierarchy.Such plug-ins form additional components (notknown to Riedl), which make developmental generegulation more multi-facetted and the resultinghierarchy more flexible; in other words, thestructure of burden in developmental processes ismore complicated than envisioned by Riedl, andthe flexibility to overcome burden is probablymuch greater than proposed by him. Evolutionarysclerosis does not seem to be a problem from theperspective of the regulatory genome.

Burden and Gradualism

By ultimately referring to Goethes idealisticmorphology, Riedl distinguished essential charac-ters (defining body plans) from nonessential ones(characters responding rapidly to selection pres-sures). At first sight, this appears to be a non-Darwinian typological perspectiveDarwin (1859)spent a considerable effort to show that unchange-able, essential characters did not exist. However,Riedl also showed how his essential charactersevolved gradually from nonessential ones byaccumulating responsibility (burden)this is agradualistic, nontypological aspect in his conceptfor the origin of body plans. Therefore, Riedl was

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not a typologist, even though he employed some ofthe traditional typological terminology.

In the modern view of body plans (Raff, 96;Arthur, 97; Gellon and McGinnis, 98), majorcharacters are still viewed as constrained, forinstance by negative pleiotropic effects on muta-tions (Galis et al., 2001). The reality of both vonBaers Law and the hourglass model (phylotypicstage) is still debated (Poe and Wake, 2004; Rouxand Robinson-Rechavi, 2008). Rather than form-ing universally accepted rules, these formalternative models of how development mightevolve. The hourglass model differs from vonBaers law in that the earliest stages of embryonicdevelopment need not be constrained, with theimplication that burden need not be higher inearlier ontogenetic events than later ones.

In recent time, homeotic mutations have beenhighlighted as potential candidates for successfulevolutionary saltations (Gould, 77, 2002; Theissen,2006), while interdisciplinary studies revealed casesthat are likely to have involved some majorheterotopic shifts (Wagner and Gauthier, 99;Rieppel, 2001). These data suggest that the rangeof mutations may be broader than acknowledged bythe Modern Synthesis. Although this has been citedin the context of the Goldschmidtian ideas ofsystemic mutations and hopeful monsters, most ofthese saltations are minor compared with the singlejumps envisioned by Goldschmidt and later postu-lated by Schindewolf for his typogenetic saltationsby which complete body plans should have arisen atonce (see below).

It is also true that most homeotic transforma-tions violate Fishers Principle (the lethality ofmacromutations) and the requirements for func-tional continuity (Budd, 2006). In a thoroughanalysis, Budd (99) showed that rather thanchanging a body plan all at once, evolution maystart at the free ends of developmental hierar-chies and then works itself upwards, until itreaches the level of body plan-defining processes.If this holds true there is a slow but successfulroute to bypass the risky ride of macromutations.Thus, even the most high-ranking burdens envi-sioned by Riedl could be changed in principle.Budds (99) mechanistic hypothesis parallels thebasic tenet of Riedl (body plan characters startsmall and free and grow large and burdened bymicroevolution), but at the same time it offers anoption for the way out of evolutionary sclerosis.How much such an upward working is alsopossible for the above-cited kernels remains anopen question.

How appropriate is the burden concept?

From the perspective of current evolutionarybiology, Riedls burden concept was right in twobasic tenets and probably wrong in a third one:(1) it was right in claiming functional continuity(body plans arise stepwise and evolutionarysuccessful saltations are unlikely), (2) he was rightin claiming that body plan characters becameincreasingly constrained by internal (stabilizing)selection, but (3) he was probably wrong inconcluding that there was no way to overcomeconstrained body plans in principle. Althoughburden unquestionably exists, its constrainingrole for macroevolution is much smaller thanthought by Riedl.

A point where Riedls burden concept may not beappropriate is his idea to measure the rank ofburden. In a perfect, rigid hierarchy of characters,as envisioned by Riedl, the hierarchical position of aparticular burden was readily identified. However,organismal traits (and the burdens they bear) mayseldom be interconnected in an encaptic hierar-chical way, but rather in complicated circuitsand feedback loops. Furthermore, each characterappears to be the outcome of geneticepigeneticinteractions, but characters themselves do not seemto have causal effects on each other directly. Thisfact makes the causality between characters muchless obvious than suggested by Riedls burdenconcept.

At present, the burden concept appears muchmore applicable to the processes of gene regulationthan to the patterns of body plan morphology.There is still a far way to go from uncoveringdevelopmental mechanisms of body patterning toan inclusive understanding of how body plansevolve. Thus, testing the reality and importance ofburden in evolutionary morphology is still out ofreach, especially when it comes to comparedifferent characters, as Riedl had in mind. Onthe contrary, regulatory networks have revealed aclearly hierarchical architecture, which undoubt-edly has an impact on evolution. The proof thatdevelopmental traits evolve at very different ratesis an important finding. It is now apparent thatthe hyperspace of states in the regulatory genomeis structured in a specific way, which does notallow evolution to proceed isotropically. In thishyperspace (or network), central regions offer lessoptions for evolution to change than peripheralregions; there appear to be given pathways forselection to act and work itself through thenetwork. This whole pattern has a lot in common



with Riedls ideas of burden in development. Thetree-like hierarchy model of Riedl has changedinto a multi-dimensional hyperspace, which natu-rally offers many more options for evolution.

ORTHOGENESIS: CYCLISM, SALTATION,AND DEEP TIME

As a passionate morphologist, Riedl (78) madeextensive reference to macroevolution, whosedescription and explanation he conceived as amajor aim of his theory. The concept of burdenwas seen by him as a key to the understanding ofmacroevolutionary phenomena such as ortho-genesis. Classically, orthogenesis lies at the heartof the idea of macroevolution, and was a majortopic in text-books before and after the ModernSynthesis (e.g., Mayr, 42, 63) as well as foropponents of neo-Darwinism (e.g., Goldschmidt,40; Schindewolf, 50). This debate had a big impacton Riedl, who was determined to form a balancebetween the Modern Synthesis and the Haeckeliantradition of recapitulation and cyclism, two ortho-genetic theories. Eventually, Riedl hoped thatthese divergent approaches would be universallyaccepted as different aspects of the same truth, allrequired to understand the full story. Althoughlong abandoned by evolutionary biology, ortho-genetic theories still have a large, implicit influencein some fields of modern paleontology, and somepaleontologists view patterns in the fossil recordin the context of such thought. It is thereforenecessary to briefly discuss these points, becausepaleontological data are becoming increasinglycited by students of evo-devo and related fields.

Originally meaning rectinlinear evolution(Haacke, 1893; Eimer, 1897), orthogenesis wasearly on coined to describe not only a pattern (anevolutionary long-term trend) but also its putativecause: internal factors as an autonomous directiveforce in evolution. Many adherents of orthogenesisbelieved that such internal factors were morepowerful than selection and often acted in opposi-tion to it. Today, the term orthogenesis is not in use(see below), but most evolutionary biologistsacknowledge that evolutionary trends exist anddistinguish various cases, such as for instancepassive diffusion and driven trends (McKinney,90; McShea, 94). These trends are generally notreferred to internal factors, and orthogenesis isrightly seen as the wrong answer to the problem ofhow macroevolutionary patterns arise. Instead,selection has been accepted as the single majorprocess for most trends since the Modern Synthesis

(Simpson, 44; Rensch, 49; McKinney, 90;McShea, 94; Gould, 2002; Hunt, 2007).

Riedl argued that orthogenesis was neither asimple macroevolutionary pattern produced byexternal selection components (Modern Synthesis),nor was it produced by factors other than selection(as non-Darwinistic concepts held). Rather, it wasthe logical consequence of high-ranking burden,which for him operated within the frame of theModern Synthesis: Riedls burden was caused byinternal selection. Riedls starting observation wasthat characters had widely different rates ofevolution, with body plan characters being themost conservative. As the fundamentals of givenbody plans could not be changed (in Riedls view),future evolution had to fit in and add to the existingframe. Hence, the dynamic pattern of orthogenesiswas a result of the static pattern of the body plan.This led him to view evolutionary trajectories asrigid and poorly flexible, which passed throughwell-defined phases that were similar across manyclades. This is the point at which Riedls original,new idea of burden met the old and troubledconcept of phylogeny paralleling ontogeny.

Cyclism

Referring to Goethes (1790) and other pre-Darwinian ideas of organic unfolding (Entwick-lung), Haeckel (1866) incorporated cyclism into hisconception of evolutionary theory. Cyclism orPhasenlehre holds that phylogeny parallels onto-geny, specifically in passing through well-definedphasesin Haeckels terms, youth (epacme), ado-lescence (acme), and senility (paracme). In thishard version, cyclism is related to a world view,according to which history is determined by specificlaws (historicism, as coined and defined by Popper,60). For Haeckel (1866), phylogeny was tightlylinked to ontogeny by means of his Biogenetic Law,which held that phylogeny was the fast andincomplete repetition of ontogeny. The hardversion of cyclism formed one of the keystones oforthogenetic theories developed in the early 20thcentury (see next section).

The concept of cyclism is not supported byrecent analyses of phylogenetic trends, and theproposed mechanisms such as the Biogenetic Lawhave long turned out to be grossly overgeneralizedand untenable (Gould, 77). Thus, the hard versionof cyclism, which was still endorsed by Riedl in the1970s (by his acceptance of the typostrophicphases described below), plays no role in modernEvolutionary Biology, and even in evo-devo there

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are no mechanisms in sight from which hardcyclism could be deduced. Therefore, severaldecades after the Biogenetic Law finally becameobsolete, Haeckels Phasenlehre remains only ofhistoric interest.

The soft version of cyclism accepts phylogeny topass through phases but rejects any internalfactors or laws involving a parallelism withontogeny. Eldredge and Goulds (72) punctuatedequilibria is a version of soft cyclism (because itpostulates the two general phases stasis andpunctuation). It may be fair to say that this issueis still unsettled (Gould, 2002), but its original,absolute claim to apply to all evolution is clearlyoverstretched and countered by evidence of ana-genetic gradualism (Futuyma, 2006). Althoughsoft and hard cyclism are sometimes confused(e.g., Erben, 88), the hypothesis of punctuatedequilibria has no immediate connection to Riedlsburden concept or the more general concept ofevolutionary constraints.

Typostrophism

Many paleontologists of the 1870s1930s adoptedHaeckelian cyclism to deduce (or rather post-dict)patterns they had identified in the fossil record(Wurtenberger, 1880; Wedekind, 16; Salfeld, 24;Abel, 29). On this background, Beurlen (26) andSchindewolf (50) developed the theory of typos-trophes. This concept involved three components:(1) orthogenesis produced by internal factors(postulated but unidentified), (2) hard cyclism,and (3) saltationism (Reif, 75, 86). In combination,this gave way to a specific macroevolutionarytheory (typostrophism) that was inconsistent withthe Synthetic Theory.

Very surprisingly, Riedl (78) employed typos-trophism to show the power of burden in channel-ling evolutionary pathways. He concluded that thepostulated results of increasing burden wereconsistent with Schindewolfs typostasis (a modi-fied version of Haeckels acme, meaning that ataxon passed through an orthogenetic phase, inwhich there was no evolutionary change except forprogression into the ever same direction). Riedlsadoption of typostrophism is remarkable, becausein his influential book, Schindewolf (50) had madeclear that typostrophism was a pattern producedby saltationan anti-Darwinian concept rejectedby Riedl. According to Schindewolf, major cladesoriginated by single jumps, which was deducedfrom von Baers Law: the more fundamental adifference between two taxa, the earlier it was

established in ontogeny. Consequently, at least inSchindewolfs line of argumentation, new highertaxa had to emerge by a punctuational change inearly development: the first bird hatched from areptile egg. Schindewolf (50) made extensivereference to Goldschmidt (40), who argued thatmacromutations (systemic mutations) were tooccur in single jumps, because his view a systemcould not be changed in incremental steps. Hencefor Schindewolf, a body plan character originatedin a single step, with the consequence that a heavyburden did not accumulate in stepwise fashion,but at once. This major difference to his burdenconcept was probably seen but not stressed byRiedl. In other words, for Schindewolf burden wasstrong from the beginning of a clade, while forRiedl it started small and grew large only aftermillions of years of evolution. In other words,Riedls understanding of typostrophes was gra-dualistic, while Schindewolfs was saltationistic.Schindewolfs typostrophe theory is today con-ceived a failed attempt to explain long-term trends,and the paleontological patterns on which it wasbased have been reinterpreted in full agreementwith the tenets of gradualism (Wiedmann, 73;Korn, 2003).

Despite the aforementioned, Riedl (77, 78)stated that typostrophism was consistent withthe hollow curves of Mayr (63). Clearly, hereferred to the pattern, not the causation assuggested by the typostrophists. Mayr (63) hadclearly emphasized the gradualistic nature ofcladogenesis and explicitly ruled out both salta-tions and internal causes for orthogenesis. Yet asmany other authors, Mayr reported cases of rapidevolutionary change followed by phases of muchslower progression, measured by the number ofcharacter transformation by stratigraphically suc-ceeding taxa, such as the study of lungfishes byWestoll (49). For Riedl (78), this was sufficient toindicate the increasing number and intensity ofburdens on phylogenetically older characters.According to him, even typostrophy, the rhythmbetween typostatic fixation and typogeneticfreedom, can be explained as the consequence ofburdened older characters becoming increasinglyfixed and conservative because of new adaptivecharacters, which build on them and at the sametime burden them again. To sum up, neithercyclism nor typostrophism form essential or evennecessary components of Riedls burden concept,and his endorsement of these theories appears toroot in the continental European tradition oforthogenesis rather than the logics of his own



theory, especially since saltationistic typostroph-ism was at odds with Riedls explicit gradualism.

CONCLUSION

Rupert Riedls concept of burden is a logicallyconsistent theory on organismic integration. Itscentral tenet is that organisms fall into hierarchi-cally nested traits that vary in their degree ofinterdependency. Burden is a measure of thisinterdependency, with the most tightly integratedtraits being the most conservative in evolution.Hierarchically nested burdens were upheld by thelong-term action of stabilizing internal selection.Although unorthodox by terminology, these viewsare consistent with the concept on internal selectionas major force maintaining evolutionary constraints(Schwenk and Wagner, 2004). Burdens are evolu-tionary constraints caused by functional interde-pendency and maintained by internal selection.

When compared with the current state of evolu-tionary theory, the burden concept holds a range ofinteresting points that may be fruitful for furtheranalysis. With contemporary evo-devo, the burdenconcept shares the focus on the evolutionary originand maintenance of body plans. It has turned outrecently that the regulatory genome is organized ina specific hierarchical way, which resembles theburden concept in some key features. GRNs(defined by all states of genes involved in theregulation of developmental processes) fall intocentral, intermediate, and peripheral domains.These domains vary with respect to their inter-connection and functional dependency, and thelikelihood of successful evolutionary changeincreases from the center to the periphery. Centraldomains (body patterning genes) are mediated byhighly interdependent networks (kernels), whichare most resistant to evolutionary change. As aresult, different organismal traits show widelydivergent rates of evolution.

Riedls burden concept differs from currentconceptions of developmental evolution in thefollowing major points.

(1) Body plans are defined by hierarchicallynested characters, which formed the focus ofthe burden concept. GRNs instead formhierarchically nested processes, which regu-late patterning, but are related in a stillunknown way to body plans. Riedls burdenwas defined on the basis of patterns, regulatorynetworks instead are made of processes.

(2) Gene regulation networks are more compli-cated (since higher dimensional) and providemore options for change than the character-based hierarchies of Riedls burden. Theburdens that constrain GRN evolution are(probably mostly) breakable, while the bur-dens that constrained Riedls body plan char-acters were not.

(3) Riedl concluded from his burden concept thatbody plan characters became increasinglyintegrated and constrained and that evolutionwithin clades was increasingly channeled.This led him to endorse cyclism (phylogenypasses through well-defined phases) and someaspects of typostrophism (evolution is directedand overly burdened body plans may faceextinction). From the perspective of modernevolutionary thought, there is no need toendorse either cyclism or typostrophism, andeven the hierarchically nested regulatorygenome allows numerous changes that grantsevolution sufficient avenues for changes insmall steps.

Future research will have to focus on therelation between the regulatory genome and bodyplans, and further down this line, interdependen-cies of morphological charactersas Riedls origi-nal focus of burdenmay come into sight. It willbe a most fascinating interdisciplinary topic tofinally analyze the burdens that shape body plancharacters. In this fast developing field, burdenmay become equally interesting as evolvability,especially when its creative aspects are analyzedin addition to its constraining effects.

The burden concept, in sum, appears to be moreinteresting and relevant today than ever before.Riedls approach was focused at an inclusiveunderstanding of causality in evolution. Any suchapproach has to keep an eye on a growing numberof factors and levels of organizationresembling awalk on a tightrope in higher dimensions. Riedlwas well aware of the difficulties of such a walk,and from the present perspective it is fair to saythat he performed quite successfully. Finally, itis befitting that with the renewed interest inintegration, constraint, and internal selection,there is also a renaissance in studying morphologyas an essential aspect of the organism. Thiswas exactly the research programme Rupert Riedlhad in mind, and for which his work, althoughit came too early and was too theoretical andmultidisciplinary for most of his colleagues, wasset out.

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ACKNOWLEDGMENTS

I thank Dieter Korn, Lennart Olsson, Wolf-ErnstReif, Robert Reisz, Adolf Seilacher, and David Wakefor very fruitful discussions. I am indebted toManfred Laubichler and two anonymous refereesfor much helpful and constructive advice.

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