Homeotic evolution in Cambrian trilobites

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2000 The Paleontological Society. All rights reserved. 0094-8373/00/2602-0005/$1.00

Paleobiology, 26(2), 2000, pp. 258270

Homeotic evolution in Cambrian trilobites

Frederick A. Sundberg

Abstract. Hox genes are known from a wide variety of organisms. In arthropods, these genes con-trol segment characteristics. Trilobites, being arthropods, probably contained eight major Hoxgenes that controlled their segment types. The trilobite Bauplan contains eight regions that are mostlikely under the inuence of one or more of these Hox genes. The cephalon contains the frontallobe, glabellar, and occipital ring regions; the thorax contains the anterior thoracic and posteriorthoracic regions; and the pygidium contains the ar ticulating ring, axial, and terminal piece regions.Changes in character distribution within or between these regions represent homeotic evolution,which may have resulted from the modication of Hox transcription or of downstream regulatorygenes. A phylogenetic analysis is used to recognize homeotic evolution in trilobites, leading to theconclusion that homeotic evolution is common among Cambrian trilobites.

Frederick A. Sundberg. Research Associate, Invertebrate Paleontology Section, Natural History Museum of

Los Angeles County, 900 Exposition Blvd., Los Angeles, California 90007.Accepted: 6 October 1999

Introduction

The importance of Hox and other regula-tory genes in a wide variety of metazoans hasreceived broad recognition by neontologists.Hox genes control the differentiation of seg-ments during arthropod development (Raffand Kaufman 1983; Raff 1996). Mutation ofthese genes, or upstream genes affectingHox genes, or downstream regulatorygenes affected by the Hox genes can result inthe transfer of a morphological feature typicalof one body region to another. For example, infruit ies ( Drosophila ), experimental manipu-lation of Hox genes has produced homeoticchange, with the generation of legs wheremouthparts or antennae belong or two pairs

of wings instead of a pair of wings and hal-teres (Raff and Kaufman 1983; Pultz et al.1988; Lawrence 1992). Mutations affecting theHox genes may be involved in the homeoticevolution of some higher taxa, including sev-eral groups within the arthropods (e.g., ony-chophorans, myriapods, insects, and crusta-ceans [Raff and Kaufman 1983; Jacobs 1987,1990; Akam et al. 1994; Whiting and Wheeler1994; Carroll 1995; Raff 1996; Averof and Patel1997; Grenier et al. 1997]).

Paleontologists, however, are only begin-ning to realize the importance of regulatorygenes in evolution. Some have suggested thatthese genes played an important role in the

Cambrian explosion and in the evolution ofseveral Cambrian arthropod taxa (Jacobs1987, 1990; Valentine et al. 1999; Erwin 1999).The intent of this paper is to illustrate that ho-meotic evolution was an important mode ofevolution for species and genera and not just

for the origin of major groups. I will illustratethat repetitive morphological features of sev-eral specic regions of trilobite Bauplan whereprobably controlled by Hox genes and that ho-meotic evolution was an important mode ofevolution in Cambrian trilobites.

Denitions

Because of potential confusion between ho-meotic change, homeotic mutations, and ho-

meotic evolution, the following denitionswill be used:1. Homeotic change (or homeotic transfor-

mation)the transfer of a feature typical ofone region or segment to another body regionor segment. Homeotic change is purely a de-scriptive term not implying a precise mecha-nism for transformation. This change can re-sult from either the mutation of Hox genes,upstream changes that affect Hox gene in-teraction with other genes (Lewis 1978; Man-ak and Scott 1994), or downstream regula-tory genes that are target genes for Hox genes(Carroll 1994, 1995; also see Budd 1999). Ho-meotic change can also result from mutation


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259HOMEOTIC EVOLUTION

of other homeobox genes not associated withthe Hox clusters (e.g., trithorax, extradenticle,buttonhead, orthodenticle, empty spiracles, Distal-less [Manak and Scott 1994 and referencestherein]). In some cases, homeotic changes canresult from environmental conditions (Raffand Kaufman 1983; Lawrence 1992).

2. Homeotic mutation a genetic mutationthat causes a homeotic change.

3. Homeotic evolution the transfer of a fea-ture typical of the ancestors body region orsegment to another body region or segment ofits descendant. Homeotic evolution takesplace when a homeotic change is heritable(i.e., through homeotic mutation).

Homeotic Change

Most discussions of homeotic changes in ar-thropods have focused on either the distribu-tion or presence of appendage and wing types(e.g., Raff and Kaufman 1983; Jacobs 1987,1990; Pultz et al. 1988; Akam et al. 1994; Whit-ing and Wheeler 1994; Carroll 1995; Lawrence1992; Raff 1996; Averof and Patel 1997), buthomeotic changes are not limited to just ap-pendages and wings. Other morphologies areinuenced by Hox genes, such as muscletypes, sternites, ventral setal bands, WheelersOrgan, anterior spiracles, Keilins Organs, andtracheal sections of the dorsal longitudinaltrunk (Lewis 1978; Raff and Kaufman 1983;Hooper 1986; Casanova et al. 1988). This is animportant point to make, for trilobites haverelatively uniform biramous appendages (andno wings), with the exception of the unira-mous antennae and the occasional uniramous

antennioform cerci (Harrington in Harringtonet al. 1959). Limb uniformity indicates that ho-meotic changes did not have a dramatic effecton the limb construction or distribution likethat illustrated or hypothesized for other ar-thropods.

Many of the homeotic changes described below are relatively minor and not wholesaletransformations. But homeotic changes arenot necessarily global; the entire set of seg-ment characteristics needs not be transferredfrom one region to another. For example, gra-dational or partial changes in segment char-acter have been documented in Drosophila(Lewis 1978; Casanova et al. 1988; Lawrence

1992). These gradational or partial changesare expected because the entire set of segmen-tal characteristics is determined by more thanone Hox gene (Lewis 1978; Raff and Kaufman1983; Lawrence 1992; Manak and Scott 1994).Minor morphological changes could also re-sult from the mutation in the binding sites ofa target gene that allowed different Hox genesto bind (Lawrence 1992; also see Carroll 1995).If this downstream gene is also a regulatorygene, then a preexisting morphological char-acter could have a new distribution amongsegments (a level 4 change of Gellon andMcGinnis 1998).

Trilobites Are Like the Rest

Hughes and Chapman (1995) suggestedthat trilobites contained Hox genes becauseHox genes are found in a wide variety of an-imals ranging from hydra, nematodes, pria-pulids, annelids, brachiopods, onychophora,arthropods, to chordates (Akam et al. 1994;Carroll 1995; Raff 1996; Averof and Patel 1997;Grenier et al. 1997; Rosa et al. 1999). Given thephylogenetic reconstruction of Annelida, On-ychophora, and Arthropoda (Wills et al. 1994,1997), trilobites contained all eight major Hoxgenes. Annelids contain ve Hox genes thatare orthologues to those found in Drosophila :labial (lab), proboscipedia ( pb), Deformed (Dfd); Antennapedia ( Antp ), and Ultrabithorax (Ubx )/abdominal A (abd-A)-like gene (Dick and Buss1994; Snow and Buss 1994). Four other Hoxgenes Sex comb reduced (Scr), Abdominal B( Abd-B), abd-A, and Ubx (the latter two replac-ing the Ubx / adb-Alike gene listed above)

are found as orthologues in onychophorans(Grenier et al. 1997). In other words, trilobitesprobably had at least eight Hox genes becausethis condition is plesiomorphic to the ony-chophoran/arthropod clade (Rosa et al. 1999).

The cheilicerate Limulus, which belongs tothe sister group of trilobites, contain either or-thologues or paralogues of at least seven Hoxgenes (Cartwright et al. 1993). Scr, which isfound in Onychophora, Hexopoda, Crustacea,and vertebrates (Carroll 1995; Grenier et al.1997), has not been recognized in Limulus. Inaddition, Limulus are reported to have fourclusters of Hox genes (Cartwright et al. 1993)instead of the single cluster found in mollusks,


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260 FREDERICK A. SUNDBERG

FIGURE

1. Regions of trilobite Bauplan where segmentcharacteristics are probably controlled by Hox genes.

annelids, crustaceans, and hexapods (Dick1997). Whether this Hox conguration isunique to just Limulus, or to all chelicerates orarachnomorphs (which includes the trilobites), is unknown.

Hox genes determine segment identity inDrosophila (Lawrence 1992; Raff 1996). Lab, pb,and Dfd regulate head segments; Scr, Antp,and Ubx regulate thoracic segments; and abd- A and Abd-B regulate abdominal segments.Because these genes are also found in a widevariety of arthropods and onychophora (Car-roll 1995; Grenier et al. 1997), we can use thephyletic phenocopy paradigm (where dif-ferences ascribable to mutant phenotypes in

model taxa are expanded in the context ofphylogeny [see Stebbins and Basile 1986;DeSalle and Carew 1992]) to say that Hoxgenes controlled the character of segmentswithin the major body sections of other ar-thropods including trilobites. Averof and Patel(1997) have documented this genetic controlin crustacean limb development. However, themorphologic expression of these genes or eventhe body regions inuenced by these genes arenot the same among all phyla (Carroll 1995;Raff 1996), or even among all arthropods(Carroll 1995; Averof and Patel 1997) or insects(Akam et al. 1994). For example, crustaceansdisplay a slightly different pattern, with Ubxand abd-A expressed in nearly all limb-bear-ing thoracic segments (Carroll 1995; Averofand Patel 1997).

Trilobite Bauplan

Expression of individual Hox genes in tri-

lobites is probably restricted to smaller re-gions of the cephalon, thorax, and pygidium.These smaller regions are based on the group-ing of similar segments within each tagma(Fig. 1). An individual Hox gene or interac-tions between Hox genes may help determinethe morphology of one or more of these re-gions. Consequently, changes in serial char-acters of these smaller regions can indicate ho-meotic evolution. The cephalon can be dividedinto three regions: (1) frontal lobe region, in-cluding the anteriormost lateral glabellar fur-row and probably the extraocular region; (2)glabellar region, which probably includes theinterocular region; and (3) occipital ring re-

gion, including the posterior border and fur-row. The presence or absence of axial nodes,axial spines, or long pleural spines in the tho-rax suggests anterior and posterior thoracicregions. The redlichiids Olenellus (Paedeumias )chiefensis and O. (P.) terminatus, both described by Palmer (1998), lack axial nodes or spines onthe rst to ninth thoracic segments; but, theyare present on the tenth to fourteenth thoracicsegments. The ptychopariid Marjumia typicalis(Resser) has a similar subdivision of the tho-rax, as evidenced by the difference in pleuralspine lengths between the rst eleven thoracicsegments and the last three segments (Fig.8A). The pygidium is also divided into threeregions that parallel in reverse order the re-gions of the cephalon: (1) articulating ring re-gion, including the anteriormost axial ring

and anterior and posterior pleural bands; (2)axial region, including the remaining axialrings and adjacent pleural eld; and (3) ter-minal piece region, which includes the post-axial area of the pleural eld.

A one-to-one correlation of exoskeleton seg-mentation to body stomites in trilobites is as-sumed (see Sundberg 1995). Thus, the regionsdened above are thought to correlate to ven-tral and internal body regions as well.

Transitional Morphologies between theMajor Body Sections

The occipital ring region of the cephalonand articulating ring region of the pygidium


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FIGURE 2. Trilobites illustrating similarities betweenadjacent regions. Anterior shaded area is the occipitalring region and posterior shaded region is the articu-

lating ring region. A, Klotziella ornata (Walcott) (drawnfrom Rasetti 1951: Plate 28, Figs. 7, 8), illustrating thesimilarity in segment character between the occipitalring and thoracic regions. The triangular raised areas(arrows) adjacent to the occipital ring, axial rings, andrst two pygidial rings are a unique conguration. Morenormal conguration of these regions is illustrated inFigure 2B. B, Niobella aurora (Westargard) (drawn fromLevi-Setti 1993: Plate 113), illustrating the similarity insegment characters between the articulating ring regionof the pygidium and the posterior thoracic region. Scale bar, 1 mm. PF pleural furrow, PBF posterior borderfurrow, AB anterior pleural band.

FIGURE 3. Proceratopyge (Lopnorites ) rectispinatus(Troedsson) (drawn from Palmer 1968: Plate 10, Figs. 1,3, 4; larger specimen has been inverted from the originalphotograph), illustrating the similarity in segment char-acter between the articulating ring and thoracic regions.The sixth-degree meraspis illustrates that segment char-acteristics are dened prior to nal tagmosis of the py-gidium. Scale bar, 1 mm. PF pleural furrow, PSpleural spine, AB anterior pleural band. Anteriorshaded area is the occipital ring region and posteriorshaded region is the articulating ring region.

(Fig. 1) have characteristics typical of the adjacent regions. Klotziella ornata (Walcott) (Fig.2A) provides a good example of the transi-tional morphology of the occipital ring region between the glabellar and thoracic regions. Inthe occipital ring region, the posterior borderfurrow is directed anterolaterally and the lat-eral portion of the occipital ring forms a small,raised triangular area on the anterior edge of

the posterior border furrow. This is a uniqueconguration for trilobites, which typicallyhave the posterior borders directed laterallyor posterolaterally and have rounded projec-tions of the occipital ring (e.g., Fig. 2B). Thisunique conguration is also present in eachthoracic segment and the rst two pygidialsegments. The anterolateral furrows or trian-gular shapes are not present in the glabellarregion or the remaining portion of the pygid-ium. Aciculolenus palmeria Chatterton and Lud-vigsen (1998: Fig. 14) is another example of in-termediate morphology between the two re-gions with its long intergenal spine identicalto its thoracic pleural spines.

The articulating ring region of the pygidi-um is most similar to the thoracic regions.This pygidial region typically has well-devel-oped axial rings and well-developed pleuralfurrows and anterior pleural bands that ex-tend to or near the pygidial margin. The sim-ilarity is most visible on species that have apleural spine on the rst segment of the py-gidium, as in Proceratopyge (Lopnorites ) rectispinatus (Troedsson) (Fig. 3), or where the re-maining portion of the pygidium is effaced, as

in Niobella aurora (Westargard) (Fig. 2B) orPlethopeltis armatus (Billings), illustrated byLudvigsen et al. (1989: Plate 45, Figs. 10, 11).In P. (L.) rectispinatus, the character of the lastthree thoracic segments and the rst pygidialsegment is dened when they are part of thetransitory pygidium. This indicates that thecharacters of these segments are dened be-fore they are released from the pygidium intothe thorax and not the result of the release it-self.

Homeotic Evolution of Cambrian Trilobites

In this study, homeotic change is indicated by distribution changes of characters among


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FIGURE 4. Representatives of Oryctocephalidae. A, Or- yctocephalites walcotti (Walcott) (drawn from Campbell1974), belonging to Oryctocephalinae. B, Arthricocephal-us chauveaui Bergeron (drawn from Chang et al. 1980:Plate 94, Fig. 1), belonging to Oryctocarinae. Scale bar,1 mm. Anterior shaded area is the occipital ring regionand posterior shaded region is the articulating ring re-gion. GD glabellar depression, GS genal spine, LGF

lateral glabellar furrow, PS pleural spine, S0 to S4lateral glabellar furrow positions (even when not pre-

sent), TG transglabellar furrow.

body segments. Only Cambrian trilobites areused here to provide examples of homeoticevolution, although post-Cambrian trilobitesprobably also display homeotic evolution.These examples of homeotic change may re-sult from mutation of either Hox genes, up-stream genes that either directly regulate theHox genes or suppress expression of segmentcharacteristics, or downstream genes affected by the Hox genes (Carroll 1994, 1995; Raff1996; Gellon and McGinnis 1998). However,the mutation type that caused a specic caseof homeotic evolution can be rmly estab-lished only when using modern organisms(e.g., Averof and Patel 1997). Therefore, when

a homeotic change is observed in trilobites itcannot be assigned to a specic mutation inthe genome.

Homeotic Evolution versus Heterochrony

McNamara (1986) proposed that hetero-chrony was a signicant factor in the evolutionof Cambrian trilobites. I propose here that ho-meotic evolution was common in Cambriantrilobites. Both homeotic change and heter-ochrony are descriptive termsthey describehow a descendant resembles its ancestor. Inhomeotic evolution, the proportion of seg-ments containing certain characters haschanged. If the segment character is either (1)deleted from one region, making it similar toother regions, yet maintained in another re-gion or (2) propagated to a new region, thenthe change represents homeotic evolution. Forexample, if a trilobite has pygidial spines andit is derived from a species that has thoracic

pleural spines and no pygidial spines, thenthe pygidial regions have obtained a charac-teristic of the thoracic region. In heterochrony,the descendant can have the retention of ju-venile features (paedomorphism) or the pro-gression of features (peramorphism) beyondthe range of its ancestor. If a segment character(e.g., pleural spines) is present within a regionat some time during the ancestors ontogeny,then the propagation or reduction of this char-acter within the region is a heterochronicchange.

However, in some instances there is no clearseparation between heterochrony and home-otic evolution. Heterochronic changes can be

the result of changes in Hox genes (Raff 1996),thereby resulting in homeotic changes. In ad-dition, some Hox genes may be expressedonly in specic ontogenetic stages (Pultz et al.1988; Castelli-Gair et al. 1994; Castelli-Gairand Akam 1995); thus, homeotic changescould result from heterochronic changes. Forexample, if the ancestor is generating pleuralspines during the formation of both the thoraxand pygidium, and the descendant generatesspines only during the formation of the tho-rax, then the Hox gene that regulated the for-mation of the spines was turned off duringan earlier growth stage before the pygidiumwas formed. However, mechanisms exist that

maintain the effects of Hox genes even aftertheir disappearance from cells (see Manakand Scott 1994).

Oryctocephalids

Homeotic changes of cephalic limbs, or atleast their muscle attachments, are well illus-trated by the Oryctocephalidae (Corynexochi-da). The oryctocephalids (Fig. 4) vary in theshape of glabellar depressions and number oflateral glabellar and transglabellar furrows.These features represent apodemes that func-tion as muscle attachments for appendages(Harrington in Harrington et al. 1959; Bergs-trom 1973; Cisne 1975). Changes in the de-


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FIGURE 5. Phylogram of Oryctocephalinae illustrating character changes resulting from homeotic evolution. Thenumber of symbols represents the number of lateral glabellar or transglabellar furrows for each node where thecounts change. The solid bar above the glabellar representation of Oryctocephalus nyensis represents a polymorphismof two or three transglabellar furrows. Phylogram from Sundberg and McCollum 1997.

pression shapes or furrow number reectchanges in appendage muscles and possiblydifferences in limb structure.

Using an explicit phylogenetic hypothesisfor the spiny oryctocephalids (Oryctocephali-nae; Fig. 4A) from Sundberg and McCollum1997 (Fig. 5), 18 instances of homeotic evolu-tion can be identied. The number of trans-glabellar furrows changed four times and is

most variable in Oryctocephalus ; O. nyensis ispolymorphic with either two or three trans-glabellar furrows. The shape of the glabellardepressions changed nine times and the ex-tension of the lateral glabellar furrows to theaxial furrows changed ve times.

This phylogram uses 36 characters, includ-ing the transglabellar furrows, depressionshape, and lateral glabellar furrows as char-acters. By including these three characters, theamount of homoplasy and homeotic change ispotentially reduced because those taxa withsimilar character states would tend to clustertogether. This study subdivides the shape ofthe glabellar depressions into three states: slit

shaped, elliptical, and circular. However, forthe construction of the phylogram (Sundbergand McCollum 1997), the elliptical and circu-lar depression shapes were assigned to thesame state because they can be distortedthrough tectonic activity.

The transglabellar furrows within Orycto-cephalus show a progressive addition in occur-rence from the occipital ring region to the pos-

terior and then anterior portions of the glabellar region. These changes are most similarto the posterior-to-anterior shift of muscle ar-rangement observed in Drosophila that result-ed from the homeotic mutation of the Ubxcomplex (Hooper 1986).

Preservation Problems. Oryctocephalid tri-lobites are typically found in deeper-water,offshore shales of the craton margin. As a re-sult, most oryctocephalids are compressed inshales, which could inuence the presence orabsence of the transglabellar furrows, shapeof the glabellar depressions, and the presenceof lateral glabellar furrows. To determine thisinuence, meraspides and holaspides of Or-


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yctocephalites walcotti Resser ( n 87), O. cf. typ-icalis Resser ( n 28), and Oryctocara geikieiWalcott (Oryctocarinae) ( n 12) from theMiddle Cambrian Spence Shale were studied.These specimens consist only of molds andcasts, typically with an authogenic mica pre-sent. No tectonic distortion of the specimenswas evident. Positive and negative impres-sions of several different sizes were studied.The location and shape of the glabellar de-pression, location of transglabellar and glabellar furrows, and cranidial length were re-corded for each specimen.

The results for Oryctocephalites walcotti areillustrated in Figure 6. Oryctocephalites walcotti

has elliptical glabellar depressions at the S0(occipital ring furrow), circular depressions atthe S1S3 positions, transglabellar furrows atthe S0 and S1 positions, and lateral glabellarfurrows at the S4 position (Fig. 4A). When ei-ther the S2 or S3 transglabellar furrows arenot clearly compression cracks but possiblythe result of compression, the box received agray shade. When the shape of the glabellardepression could not be accurately deter-mined because of compression or preserva-tion, the depression shape is recorded as anopen circle or ellipse.

The results illustrate that the shape of glabellar depressions and presence of transglabellar furrows are consistent through devel-opment and compression. The shapes of theS0 glabellar depressions were difcult to de-termine only in the smallest specimens ( 1.6mm; see below). Only a few specimens devi-ated from the standard form given above,

and most of these are questionable and couldhave resulted from compression (gray boxes).Two examples (2.02.2 mm and 3.03.2 mm, both in the rst row) are notable exceptions,they have well-developed transglabellar fur-rows not only at the S0 and S1, but also at S2and S3 positions. Another specimen (5.65.8mm, second row) has the transglabellar fur-row missing in the S1 position. These rare oc-currences represent homeotic change withinthe species.

In addition, although not presented on Fig-ure 6, the number and location of the lateralglabellar furrows are also consistent in thelarger specimens (see below).

Similar results were obtained for Oryctoce- phalites cf. typicalis and Oryctocara geikiei. Theglabellar depression shape and location oftransglabellar furrows were constant, withonly a few questionable deviations from thestandard forms. This study suggests thatcompression does not mask these individualcharacters.

Homeotic Evolution versus Heterochrony Revis-ited.Meraspides and holaspides of Orycto-cephalites walcotti, O. cf. typicalis, and Orycto-cara geikiei typically do not display ontogenet-ic changes of the character states discussedabove. Meraspides of Oryctocephalus indicus(Reed) (redescribed in Sundberg and Mc-

Collum 1997) also show no ontogeneticchange in these characters (Sundberg unpub-lished data). Because these oryctocephalidsare generally consistent in the number orshape of glabellar depression, transglabellarfurrows, and lateral glabellar furrows duringontogeny, specic changes in these features donot represent heterochrony.

The smallest specimens of Oryctocephaliteswalcotti are an exception. The elliptical de-pressions in the occipital ring furrow (S0) ofthis species appear to be slit shaped in ce-phalon sizes between 0. 8 and 1.4 mm (Fig. 6),although the slit shape could not be rmly es-tablished and can be the result of preservation(see above). The adaxial portion of the occip-ital furrow (S0) in these smaller specimens ispresent, indicating an ontogenetic loss of thisfeature in holaspides. These results indicatethat heterochrony may be responsible for thechanges in depression shape and in the ad-

axial furrows for the occipital ring region, butnot for observed changes to the anterior.Other Trilobite Groups. The cranidia of Or-

yctocephalinae provide us with a set of uniquemorphologic characters that illustrate home-otic evolution. Other trilobites possess some ofthese cranidial features, although no othergroup has all three characters developed asextensively. Glabellar depressions are presentin ptychopariids (Phacopina, Olenacea) andredlichiids (Olenellina, Redlichiina). Trans-glabellar furrows are common among the red-lichiids (Olenellina, Redlichiina, Bathynotina), but rare among the ptychopariids (Ptychas-pidacea). Lateral glabellar furrows do not con-


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FIGURE 6. Histograms illustrating the presence or absence of transglabellar furrows (curved line) or circular orelliptical glabellar depressions (circles or ellipses) in individual specimens of Oryctocephalites walcotti. Individualspecimens are represented as a box in the same position in each histogram. The curved line in a box indicates thepresence of a transglabellar furrow in that specimen at that glabellar position (S0S3). Gray boxes indicate ques-tionable presence of transglabellar furrows due to preservation. Circles or ellipses indicate the glabellar depressionshape in that specimen at the position. Solid circles/ellipses indicate positive identication of depression shape,and open circles/ellipses indicate questionable identications due to preservation. Arrows indicate specimens thatdeviate from the standard form of the species.


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FIGURE 7. Specimens of Nephrolenellus showing differ-ences in node (N) distribution in the glabellar and oc-cipital ring regions. A, Nephrolenellus multinodus (Palm-er), drawn from Palmer and Repina 1993: Fig. 4.4. B, Ne- phrolenellus geniculatus Palmer, drawn from Palmer 1998:Fig. 6.1. Scale bar, 1 mm. Shaded region represents theoccipital ring region.

nect with the axial furrows in several ptych-opariids (some Phacopina, Proetacea, Cerato-pygacea, Remopleuridacea, Anomocaracea,Olenacea) and redlichiids (Olenellina, Redli-chiina). Oryctocephalids are unique amongthe corynexochids in possessing these glabel-lar characters. A precursory survey suggeststhat good examples of homeotic evolution ofthese glabellar characteristics are presentwithin the redlichiids (Olenellina, Redlichi-ina) and ptychopariids (Olenacea).

Axial Nodes

Axial nodes or spines are common on sev-eral trilobites, including some redlichiids (El-

lipsocephalidae, Olenellina, Redlichiina), cor-ynexochids (Dolichometopidae, Dorypygidae,Zacanthoididae), and ptychopariids (e.g.,Alokistocaridae, Cedariiidae, Dikelocephali-dae, Idahoiidae, Marumiidae, Parabolinoidi-dae, Ptychpariacea, Saukiidae). These nodesoccur on the axial rings of the occipital ring,anterior thoracic, posterior thoracic, articulat-ing ring, and/or axial regions. Distributionchanges in these nodes represent a homeoticchange. For example, an ancestor could have anode on the occipital ring and its descendanthave nodes on the occipital ring and thoracicrings, indicating the thoracic segments acqui-sition of the occipital ring feature.

Perhaps the most interesting distribution ofnodes is seen in Nephrolenellus multinodus(Palmer). This species is unlike any other ole-nellid in its possession of axial nodes in theoccipital ring and glabellar regions (Fig. 7A).The stratigraphically younger Nephrolenellus

geniculatus Palmer generally lacks the nodeson the glabellar region (Fig. 7B), although thesmaller specimens do have a complete set ofaxial nodes (M. Webster personal communi-cation 1999). If the younger Nephrolenellus isthe descendant of the older species, then twohomeotic changes have occurred: the glabellarregion acquired the node typical of the occip-ital ring region in N. multinodus, and then thisfeature was lost in N. geniculatus. This nodeloss appears to be tied to a heterochronicchange as well.

Palmer and Repina (1993 and gures there-in) provide various examples of homeoticchange in the distribution of axial nodes in

olenellids. Several species have no axial nodeson the thoracic segments (e.g., in Fig. 4, Bice-ratops nevadensis Pack and Gayle, Peachella id-dingsi [Walcott], Bristolia bristolensis [Resser]).Some species have nodes on all thoracic seg-ments (e.g., in Fig. 3, Mummaspis occidens [Wal-cott] Olenellus (Olenellus ) thompsoni [Hall], andOlenellus ( Mesolenellus ) hyperborea [Poulsen]).Still others have nodes on only the posterior

thoracic segments (e.g., in Figs. 3 and 4, Ole-nellus (Paedeumias ) transistans [Walcott] andGabriellus sp.). Lieberman (1998) consideredthe presence of axial nodes as plesiomorphic(his character 66, state 0). The disappearanceof all axial nodes on the thorax occurs fourtimes on his cladogram of the olenellids (char-acter 66, state 1). Axial nodes are present onlyon the posterior thoracic region two times onthe cladogram (listed as character 66, state 0).The disappearance of axial nodes from eithersome or all thoracic segments and their per-sistence on the occipital ring (Lieberman 1998,character 40, state 1 or 2) represents homeoticevolution within the Olenellinae. The number


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FIGURE 8. Specimens of Marjumia showing differences in pleural spines and pygidial spines. A, Marjumia typicalis(Resser), drawn from Levi-Setti 1993: Plate 107. B, Pygidium and thoracic segments of Marjumia masoni (Resser),drawn from unpublished gure. C, Marjumia laevinucha Robison, drawn from Robison 1971: Plate 90, Figs. 1113.Scale bar, 1 mm. Anterior shaded area is the occipital ring region and posterior shaded region is the articulatingring region. Specic thoracic segments are numbered. PS pleural spine.

of episodes of homeotic evolution within theOlenellinae is difcult to determine becauseLieberman (1998) used only one representa-tive of each genus in his cladistic analysis.Node appearance on thoracic segments is var-iable within genera as well as between genera(see Palmer 1998).

Pleural SpinesSeveral trilobite groups also display home-

otic evolution in the distribution of pleuraland genal spines. Oryctocephalidae not onlyhave the typically spiny forms that were dis-cussed above (Oryctocephalinae, Fig. 4A), butalso nonspiny forms (Oryctocarinae, Fig. 4B).The spiny forms typically have long genal,thoracic, and pygidial spines. A few taxa inOryctocarinae have lost some of these spines.

For example, Oryctocara ovata Tchernysheva(1962: Plate 4) has small pointed terminationsof the thoracic segments but lacks genal andpygidial spines. Tonkinella also has smallpointed terminations of the thoracic segments but possesses long genal spines much like Or-yctocephalinae (see Rasetti 1951: Plate 31, Fig.14). Other members of Oryctocarinae have lostall spines, for example, Arthricocephalus chau-veaui Bergeron (Fig. 4B), Oryctocara geikiei(Walcott) (see Whittington 1995: Plate 4), andSandoveria lobata Shergold (1969: Fig. 14). Thisprogressive loss of spines probably representshomeotic evolution, although the phylogenyof this group needs to be worked out before

the number of episodes can be determined. Inaddition, the nonspiny Oryctocarinae are var-iable in the number and/or shape of the trans-glabellar furrows, glabellar depressions, andlateral glabellar furrows, as are the spiny Or-yctocephalinae, and probably display home-otic evolution in these characters.

The presence of pygidial spines in somespecies of Marjumia (Marjumiidae, Ptychopa-riida) and their absence in other species (pre-viously assigned to Modocia [Melzak and Wes-trop 1994]) (Fig. 8) provides another exampleof homeotic evolution. These pygidial spinesare the propagation of thorax type spines ontothe pygidial regions and not the fusion of athoracic segment to the pygidium. If the py-gidial spines resulted from the retention ofthoracic segments within the pygidium, then

the spiny taxa should have fewer thoracic seg-ments and more pygidial segments. Taxa thatlack pygidial spines have 12 to 14 thoracic seg-ments and 3 to 4 pygidial axial rings (Robison1964, 1971; Schwimmer 1973). However, thespiny species has 14 thoracic segments and 3to 4 pygidial axial rings (Robison 1964), andthus the presence of the pygidial spines is theresult of homeotic change. If thoracic seg-ments were being retained in the pygidium,then forms of Marjumia with only 13 thoracicsegments should have a set of pygidial spines,which they do not (Fig. 8C).

Lengths of thoracic pleural spines also varywithin Marjumia. Marjumia typicalis (Resser;


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Fig. 8A) has long pleural spines, increasing inlength from the rst to the eleventh thoracicsegment (anterior thoracic region) and muchsmaller pleural spines on the twelfth to four-teenth segments (posterior thoracic region). Marjumia masoni (Resser) has a similar in-crease in pleural spine length, but the last fourthoracic segments decrease in size graduallyand the rst pygidial segment has a smallspine and looks much like a thoracic segment(Fig. 8B). Both species differ from M. laevinu-cha Robison (1971) (Fig. 8C) and M. brevispinaRobison (1964: Plate 87, Figs. 1119), whichhave only rounded pleural terminations.

Discussion

The taxonomic importance of the charactersdiscussed above for Cambrian trilobites islimited. Taken by themselves, homeoticchanges in glabellar depressions, transglabel-lar furrows, lateral glabellar furrows, pleuralspines, and axial nodes are used to dene dif-ferent species or genera, but not higher taxa.On the other hand, thoracic segment types(prothoracic versus opithothoracic segments)and the presence or absence of genal spinesare used to help differentiate two subfamiliesof Olenellina (see Palmer and Repina 1993).The depth of lateral glabellar furrows, thepresence of thoracic pleural spines, and thepresence of pygidial spines have been used tohelp differentiate between families of ptych-opariids (e.g., Robison 1988; Ludvigsen et al.1989) and corynexochids (e.g., Chang et al.1980; Whittington 1995). Further investiga-tions may determine if these character chang-

es are the result of homeotic evolution and ifhomeotic evolution was in part responsible forsome Cambrian supergeneric taxa.

Jacobs (1990) suggested that homeoticchanges played an important role in the evo-lution of Bilateria in the early Phanerozoic.His work predicts that homeotic evolutionshould have been more frequent in the earlyevolution of arthropods because of the relativesimplicity of gene regulation and the closespacing of Hox genes on the chromosome.This work provides a framework to test Ja-cobss (1990) hypothesis. Homeotic change ispresent in the evolution of Cambrian trilobites, and this study suggests that it may be

widespread. Further work on both Cambrianand post-Cambrian trilobites would help de-termine if homeotic evolution was more im-portant in the early Paleozoic than in latertimes. Do post-Cambrian trilobites displayhomeotic evolution as often as Cambrian tri-lobites? Do Early Cambrian trilobites displaymore homeotic evolution than Middle or LateCambrian trilobites?

Summary and Conclusions

Eight Hox genes are plesiomorphic to ony-chophorans and arthropods; thus, trilobitesprobably had all eight Hox genes. The trilobiteBauplan displays patterns of segment types

that are consistent with the idea that trilobitesegment morphology was controlled by Hoxgenes. These Bauplan patterns are used to de-ne eight regions, which are identied here bythe axial and pleural areas. These are the (1)frontal lobe (2) glabellar, (3) occipital ring, (4)anterior thoracic, (5) posterior thoracic, (6) ar-ticulating ring, (7) axial, and (8) terminal pieceregions. The occipital ring and the articulatingring regions are transitional in morphology between the adjacent thoracic and either theglabellar or axial regions.

Unique characters are used to documentseveral instances of homeotic evolution withinCambrian trilobites. In the oryctocephalids,homeotic evolution is widespread, as deter-mined by the distribution of transglabellarfurrows, lateral glabellar furrows, glabellardepressions, and pleural spines. A brief sur-vey also indicates that Cambrian ptychopa-riids, redlichiids, and other corynexochids

also display homeotic evolution with the re-distribution of pleural spines and axial nodes.Homeotic evolution is common in Cambri-

an trilobites, at least on the specic and ge-neric levels, and may have had a hand in theevolution of supergeneric taxa. This work alsosuggests that paleontologists should explorethe potential of homeotic evolution for othertaxonomic groups.

Acknowledgments

L. and V. Gunther kindly provided the or-yctocephalids from the Spence Shale. G. Budd,D. H. Erwin, N. L. Gilinsky, N. Hughes, D. K. Jacobs, R. Jenner, D. Johnson, and F. R. Schram


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provided many helpful comments and discus-sions relevant to this paper.

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Homeotic evolution in Cambrian trilobites

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