Functional Morphology and Diversity

Functional Morphology and Diversity

The Natural History of the Crustacea, Volume 1

EDITED BY LES WATLINCs AMD MARTIN TIIIEL

oxroRi) \ ' S ' J't ' • I COMMENTS ON CRUSTACEAN BIODIVERSITY AND DISPARITY OF BODY PLANS

Frederick R. Schram

Abstract

The scicnce ofnatural history is built oo twin pillars: cataloging the species found in nature, and reflecting on the variety and function of body plans, into which these species fit. We often use two terms. dtrcnily and disparity, in this connection, but these term; arc frequently used inter- changeably and thin repeatedly contused in contemporary discourse about issues of function and form Nevertheless, diversity and disparity are distinct issues and mutt be treated as iucb; each influences our views o: the evolution and murphoiogy of crustaceans.

CRUSTACEAN DIVERSITY

Crustaceans exhibit great disp«rity in basic body plans {1 return :o this subject below), but disparity of crustacean form is different from crustacean biodiversity, that is, the number of specie) wo have within any particular group. No one knows lor certain the exact number of species within any group of organisms, although the situation might improve with the appear- ance of online catalogs for particular groups. The people who set up these databases and maintain them as new species arc added and old spccics arc placcd in synonymy provide a much-necded service toward adequately cataloging the tree of life. Nevertheless, as huoians wc like numbers—they are easily understood. So 1 have made my own tally (Tahle 1.1) and present a summary of estimates compiles) from various authorities as to the total number of crustacean species.

There is clcatly no agreement on numbers amor.? the authors listed in Tabic l.i, although tbr estimates have gpne up through time. With the exception of Minelli (1091) and Brusca and

hmtmudUerrMt/ymol Din-Mr.. Id.'id La W*ling and Martin Thirf © joyoilord Uflivfsiiy Press l"uWi"l»»

" fclc Various estimates of global numbers of $pccies of crustacean*.

F-stimated nambci of tpeciei Sourer •14,950 Bouchet (1006) J!,000 Brusca and Brusca (1990) 68,171 Brusca and Brusca (:ooi) 40,000 Groombridge and Jenkins (1000)

$9,000 May (19S8) 75,000 Meglitsch and Schram (1991) SSJ<*4 Minelli (1993) 58,000 Ruppert and Barnes !i?9*) 49,658 This chapter

Brusca (zooj), who appear 10 have attempted a real count, ihc other authors obviously provided rounded oil and rough estimates. i:or example, the number provided by Meglitsch and Schram (1991) was an estimate of what the highest number might be at some point :n time when knowl- edge o^tbc number of species will have reached a plateau.

Although we know a great deal about groups of invertebrates, our knowledge is not very good and rather incomplete. 1 eiamined the patterns through time in documenting animal taion diversity {Schram 1003) and noted several periods during which plateaus of relative inac- tion followed bursts in activity. It seems clear from these charted patterns that we are currently in one of those periods of increased activity, but whether we will soon reach a new plate-au, or whether increased use of molecular techniques to identify monophyletic groups might con- tinue to add new taxa at all levels—from phylum down to species—I cannot say. However, increasing application of molecular techniques does seem to indicate that we have underesti- mated the degree ol cryptic speciation in nature.

Having stated this, I feel honor bound by the charge given to me by the editors to provide my own numbers, so 1 tally here the currently known crustacean species. Table 1.2 is based on a census O- relevant websites, currently available monographic literature, and the best estimate! of authorities active in one or more of these groups. The reader should keep in mind that this is a tally of species numbers at this point in time, and these figures can only increase as our knowledge of these taxa evolves. In fact, the survey made by Martin and Davis (joo6) seems to Indicate that no asymptotes arc yet emerging in the pace at which new species are being described.

First, the total number of specses obtained by this survey, 49,058, is not too far off from the estimates of ilouchct (aoois) and Minelii {1993). Within that number, some things deserve spe- cial notice. Of the two largest groups on this list, Manllopoda and Malacottraca, the numbers arc of similar magnitude—almost -.9,000 and something more than 19,000, respectively. The number of maxillopodans can only increase. The 9,500 copcpods is only an estimate, although it may stand close to the actual numbers of currently described species. Nevertheless, copepod taxonomy is an active discipline, and increasingly sophisticated techniques of study will help isolate cryptic species. The 8,oo# species of ostracodes is only an estimate, and if we factor in fossil species, we would mote than double that number. Furthermore, the application of molecu- lar methods in Crustacca will likely alfect our understanding of species level biodiversity. For example, I am surprised at the relatively low number for the thecostracans, but parasitism is rampant in the group, and underestimates oftpecies diversity would prevail in taxa with such Crustacean Biodiversity and Disparity of Body Plans 3

7-b:.e 2. Census of species numbers in various crustacean groups.

J'axon Number of species

Branchiura (Argulida) >75 Branchiura {Pcntaslontida) 100 Mystacocarida «J Ri anchiopoda 509 Anostraca J07 Cyclcst herida I Laevicaudars 36 Noiostraca 'S Spinicaudata =ISo Cladocera Maiillopoda Copcpoda iS,9ii Ostracoda 9,500 Myodocopida *8,oo8

Podocopida 1,608 (*500 fossils)

Thccostraca 6,400 (-9,500 fossils) Ascothoracica Cirripedia >99

'.304

Acrothoracica >61 >l Rhizocephala 55 Thoracica 948 Faeetotccta I* Tantulocarxia 18 Remipcdia '9 Cephalncarida 10 Maiacottraca Phyllocanda Stomatopoda 19 Eumalacostraca 456 Syncanda J8,9?6 >187

Bathynellacea >170

Anasp.dacca 17 Peracarida 15,686 Amphipoda 6.950 Cumacea W Isopoda Lophogasirida 5/170 Mictacea 46 Mysida sensu lata s Mysida jensu SirlCtO 1.085

Stygiomysida 1.075

Spdaeogriphacea 10

Tanaicacea 4

940 4 functional Morphology and Diversity

Table 1.2. (Continued)

Taxon Number ol species Thermos bacoacca M Eucarida ll.iOi Amphiomdacea 1 Decapoda >i/>i6 Dendrobranchiata ill Caridea •750

Stenopodidea 57 Reptantia 9.-707 EuphausiaCea 86

Total «9.6sS

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highly reduced body forms. For example, rhixocephalans seem polled on the edge or .1 renais- sance in interest, and the number of species anticipated will increase.

MaldCOStraCa constitutes a large number of species, but the species distribution is uneven because some subgroups arc very large (amphipods, isopods, reptant decapods), while others are small (mictaceans, spclaeogriphaceans, and theamphionidacean). In fact, any group associ- ated with cave or groundwater habitats appears likely at the lower end of species number esti- mates but these habitats are difficult to study, and every attempt to sample these communities turns up new and interesting species, which can only continue into the future. {In this connec- tion, one need only'consider the work on crayfish in North America to sec what happens when intensive systematic interest is focused on a group.)

Some major class- and order level taxa presently have low species numbers (rcmipedes and cephalocarids), but here, too, we have animals living in habitats that are difficult to sam- ple (anchialine caves and the deep sea). Other groups contain very cryptic creatures living in places that, although well studied, nevertheless are olten overlooked (mystacocarids in inter stitial beaches).

Because ol the great disparity ol body plans exhibited by crustaceans, we have a problem in comparing the species numbers in one group with another The taxa in Table i-i are organ- ized around the currently recognized class and order levels, but how does one compare ordi- nal differences seen in malacostracans with what are called orders within the maxillopodans? Recognizing a decapod from an amphipod is quite easy (both arc orders of F.umalacosrraca), but not many people could easily distingu ish a cyclopoid from a caknoid (they are both orders of Copepoda) without being carefully schooled in the differences. Hence, trying to compare numbers of species within groups across the major taxonomic (class-level) units of crusta- ceans is truly like comparing apples to oranges or, in this case, lobsters to zooplankton.

Nevertheless, strange patterns arise when we look within groups. Consider the petacari- dans. for ex.mplc. Why are there so many species of amph.pods (6,900) compared to thcr- nvosbaenacraos (n) o, mictaceans (s>-appro«,m..ely two and three orders of magnitude difference? Are amph.pods truly that much better adapted to their environments, an expla- nation often assumed to be true? If so. how and why? Or, are some other factors at play that might augment or possibly even ignore issues of adaptation? Some of these factors might be Crustacean Biodiversity and Disparity of Body Plans 5

Number oi specits In germs

Fig. l-i. Arithioetx hollow curve (A) ar.d log-leg (8) plots of sire distributions of genera Ot Stomitopoda (» number or included ijxi.es) roughly conforming to power law N{x) - flX"'. Foe details about the method. secMinelliet »l. Ow)-

difficulty of habitat access for study (mentioned above), age ol a clade, habitat heterogeneity, and expressions of chance in nature. The various authors of other volumes in this series will explore many of these issues.

The element of chance plays an important role in classification. Willis and Yule (19") and \iinoli 1 et al. (1991) observed that the size o: supraspecific taxa as related to the included sub taxa (species in genera, genera in families, etc.) follows a power law. They concluded rhat the structure of biological classification is naturally fractal. This structure can be expressed as a hollow curve that, if plotted on a log-log scale, would conform to N(x) - ax *.

We can Illustrate this with one example from Malacostraca, the umpeltate stomatopods (mantis shrimp). As of this writing, we re genera of mantis shrimp, with an additional 113 nominal species currently in synonymy. It we consider only the 456 rec- ognucd spccies, distribution numbers range from one of the largest genera, Nannaquilla, with some 16 species, down to >£• genera w-th but a single species each. Graphing this diversity, we can see that on an arithmetic scalc it forms a hollow enrve (Fig. 1.1 A), and on a log log plot a 6 functional Morphology and Diversity

Straight line emerges (Fig. i.:B). The fractal pattern becomes apparent when examining genera within families (data not shown), where we would again sec a log-log plot that roughly matches that ol species in genera. Whether this pattern appears in othergroups of crustaceans remains to be tested, but I have no doubt that it will hold is it has m other groups of animals aod plants.

As humans, we are naturally inclined to seek causative explanations for patterns of biodi- versity. However, I believe we do not necessarily need to explain why one particular genus, such as Nannotquilla with x6 species, is somehow better adapted than its confamilial sister genera, in this case Mextsquilta and Kcpptlius, each with only a single species. As we chart spe- cies biodiversity, we should be open to the possibility that the relative number of taxa within any particular group may represent nothing other than the manifestation of the operations of a stochastic, fractal universe, to Say nothing ol the vagaries ol individual taxonomic decisions. Many authorities might reject my pessimism here, but at the very least, a stochastic, fractal biodiversity has to be one of several alternative hypotheses to consider.

CRUSIAQAN DISPARITY OF BODY PLANS

The crustaceans are the most variable of all the arthropod groups; that is, there is a great dis- parity of body plans throughout their ranks (Fig, i.i). If we are to assume that Crustacea is a monophyletic group, then they are not like any other arthropods. This h igh degree of vanabil ity is a very real problem with some serious implications, because if we take this disparity of form at face value, then we should seriously question whether all these various groups can constitute a single monophyhim.

When one looks at other major arthropod groups outside of Crustacea, there appears to be no great disparity of plan within these taxa (see Meglitsch and Schram 1991); members of each group fit a concise definition. For example, members of Insecta (Hexapoda) have a body divided into a five-segment head with tl>e first postantennal segment bearing appendages modified as a labrum, a three-segment thorax with two sets of wings in the pterygote bisects borne on the second and third segments, and an abdomen of 10-11 somites. All insects conform to this defini- tion with some exceptions, for example, allowing for fusion of segments at the terminus of the abdomen or modification ol wing arrangements. Insects have a unified body plan.

Myriapoda as a whole do vary m some features such as body length but have io common that their trunk is not divided into a thorax and abdomen and that their gonopores are gener- ally located on theantenor aspect of the trunk. The individual gioups of myriapods conform to common plans: Syraphyla have 1; trunk segments with the gonopores on the fourth somite; Pauropoda bear u trunk segments with the gonopore on the second somite; and Diplopoda, with several very distinct orders, all exhibit well developed diplosomites, that is, pairs of seg- ments fused dorsally but distinct ventrally, and their gonopores are located on the second trunk segment. The individual orders of diplopods vary only regarding the total number of trunk somites.- pselaphognaths have at least 10-1 j, but colobognaths can exceed 30. Chilopoda have variable trunk segment numbers, extending from 15 to more than 180 pairs of legs, depend- ing on group, but all chilopods without exception have long antennae and modify the first trunk limb as a fang equipped with a poison gland to facilitate their earn ivory. Centipedes alto uniquely bear gonopores on die posterior aspect of the trunk.

The subphylum Chdicenformes exhibits only a few "head" segments, essentially two, and these are fused with the anterior, or loeomotory, part ot the trunk to form a prosoma. The ante riormost somite (the one just posterior to the asegmental acron), the homnlng of the antcnnal segment in other arthropods, does not carry antennae but rather is equipped with a pair ofche- licerae. The second segment, what in other arthropods is referred to as the first postantennal Crustacean Biodiversity and Disparity of Body Plans 7

Fig.i.i. Ditpirare body types among crustaceans.

segment, typically bears a well-developed set ot l.mbt, .ilbcit variously developed. There are no exceptions to this basic format.

Within the chcliceriforms. the highly distinctive Pycnogonida appear to be all legs, their prosoma ieduced to a thin cylinder. The mouth »located terminally on a long probowiS. The small turreted "head' beats cbeliccrae, a second >.rt of limbs called palps, and a third set of limbs modified as ovigers in the males. Posterior to these limbs, roost pycnogonids utilize four pairs of lep for locomotion (a few forms wit n five or six pain are known). All sea spiders con- form to this body plan.

Aradmida ha«T a sii-vrgwnl protoma, with eheltferae. redipaips. aad focr pa.rs of ««i fe- rn* The troftk bears an addeioeal optsthoioau of divers* fonn b«*t composed**sorae ij somites, with the first segment greatly reduced inn -trow pedicel and the .second bearing the gonopore*. OpisthosomaJ limbs are missing oe greatly reduced. Despite a great variety of body profiles, especially regarding the opisrhosoma. all arachnids conform to this single plan.

Merostomata, a small group today, was moie extensive (and diverse) in the past. The prosoma bears six pairs of limbs. The chelicerae arc followed by four sets of modest-sued walking limbs with specialized gnathobatei, the first of wh.ch in the males is modified for 8 functional Morphology and Diversity

grasping the female during copulation, and a somewhat larger fifth set effective in groom mg the underside of the prosoma. The next somite, the pregenital segment, is reduced but bears mod.fied limbs, the chiiaria. Unique among living chcliceriforms, the opisthosomc of the merostomes bears six pairs of limbs postenor to the genital segment. All merostomes conform to this plan.

From this short review, we can see that all these groups of arthropods have conc.ce diag- noses, with distinct sets of apomorphies that character all members of the group. Crustacea, if vie wed as a single group, simply docs not have this.

CAN WE DIAGNOSE A MONOPHYLETIC CRUSTACEA?

Any invertebrate zoology textbook can provide a set of characters for Crustacea. When 1 was «*ed to provide such a diagnosas ,5-50 years ago (Schram 1,79, -982), I certainly did not hesi- tate. However, we now realize it is not sufficient to simply string together any list of characters. Ideally, as in the arthropod examples cited above, these characters should be unique derived features that diagnose a II members of the group. To rephrase this in contemporary terms, a diag nos.s should offer synapomorphtes that together uniquely delineate a monophyletic grouo. We Strive for natural taxonomy, classifications that reflect evolution. It is critical to determine if this is possible for Crustacea.

A commonly accepted diagnosis of Crustacea consms of the following: (,) head of five somites, each bearing a set of appendages consoling of two pai/s of antennae, a pair of mandi- bles, and two pairs of mailllae; (a) body consisting of three regions: head, thorax, and 'abdo-

men'; (j) trunk appendages primitively multiramous; and (4) development consisting of a Ser.cs of discrete larval and/or juvenile stages, initiated by a stage termed a naup!,ut.

Let us inspect these features one by one in order to determine if these characters provide that unique set of descriptors we require for a diagnosis of Crustacea. In the discuss**, below, I

restrict the term Ou,r«M to mean a monophyktic group and the term mauuwmorph to con- note the amalgam of arthropod types that we generally and broadly refer to as •crusticeans" (fossil and recent) bu: that may or may nor be monophyletic. Table 1., will assist the reader in following along the taxa and many of the relevant features discussed below.

"Head of five somites, each bearing a set of appendages consisting of two pairs of antennae, a pair of mandibles, and two pairs of maxillae"

These are not a unn,ue set of features. A head consisting of five somites is shared with insects and the mynapods (see above; Meglitsch and Schram ,99.), and, as would follow, moil of the head appendages of these somites ate shared among the three groups, namely, die first set of antennae, mandibles, and two sets of maxillae. It is only regarding the So-called second set of

antennae that we might have a distinctive crustaceomorph feature 4incc myriapods and insects lack a limb in this position

The second antennae arc geneially perceived as iptciah^d sensory limbs and as such could serve asa dcfm.ngapomorphy. This descriptor arises from the mental image of Crustacea con- luted up by thinking of a shrimp or a lobster (a malacostracan), and this image w.thout a doubt presents us with an icoo of an arthropod with a set of sensory limbs at this position, albert with slight anatomical variations, depending on group (Fig. i.jA).

Nevertheless, sensory second antennae are not characteristic of all groups of crustaceo morphs. Chapter 7 provides additional details Concerning antennae, but a short overview will suffice here to make a point. Recedes have quite distinctive limbs in this position (Fig. ,.,B) that I suspect serve equally as a hydrofoils to direct currents of water that flow ii

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Fig. I.J. Viriou. functional tvp« o1 "antennal" limbs found in crustaceans. (A) Sensoiy. AfUuJti kirmaphro- Uilnui. lanjx) (from Lang 19s)). (B) Swimming hydrodyaainic plant L+uvnnU% r*lr>cho«.i a rt impede (Ifom Schram«« «l >«*«). (C C") Ueomoeocy/feedlng: DeedinicMr,, i^gr-i. a myitaco. ((-.-n I Imkt 1909). «mrana (C) and mand.Nc (CO- The irr» radicates gnathal !ob««. (D) Put ad an attach nunc cocipJri^ , Brancfciuraa (from Vartin -9)1). (E) S-intmmg. A/ctomuuf^ui ittryl.. »op*pod (from Poxshill (f) Hou p»octr«tOT: Gcrjcnoriinmo mus,Ui, in .wodmraodan (Jnm Grypo ^ (C) Wn-.^ fr.daj » s.i>Uopod*o (fro- Mail.. m>J W.Unwk I9$tl

• 1 mind the head and perhaps alio to aid in creating some of those currents by flapping the hydroplane-like exopods. Although no work has yet been done on functional morphology of thu limb, I believe it safe to say that the rcmipcde antenna is not a purely sentory append- age Mystacocarids have a pair of limbs behind the first antennae that are virtually identi cal in torm to the mandibles (Fig. i.$C,C'), except these so-called second antennae lack the gnathal armament at the base of the limb that occurs on the mandibles. The myitacocarid "antennae" are locomotory limbs. Rraochiuraas possess broad plates in this position with basal honks and terminal, recurved spines—nothing sensory at all but rather serving to assist with attachment (Fig. i.jD). Tantulocands lack head appendages altogether. Copepuds have well-developed limbs in this position that serve for the most part as the primary organs of swimming (Fig. ijE). It is difficult to specify what this limb does in ascothoiacMaiu, whete Crustacean Biodiversity and Disparity of Body Plans 11

ill head limbs are highly modified to achieve attachment to a host or lo penetrate host tis sues (Fig i.jF). In cirripedes. the adults lack the antennae, but the nauplius and cypris lar vae have limbs in this position to aunt in swimming; the second antennae disappear at the time of attachment prior to metamorphosis to the adult cirr.pcdc Finally, within the wide array of Cambrian miCroarthropods that are considered to bear some relationships to modern gro>|» (*ee chapter i). soch as BnLsaeu (Fig. i jC), RtkhuktUa. Stara. and

Walaittkia, the so caGed second antennae are more orten than not locomotory limbs, similar in structure to the mandibles and maxillae of these fossils.

We can conclude from this brief mrvcy that the only character that Crustacea share at this position, that is, the first segment posterior to the true antennae, is simply the p'fSrn.v oja pair oJUml». However, this is to say nothing—the mere presence of limbs on the first postantennal segment, or any postantennal segment for that matter, is a generalued, prinMtive,orplesiomor phic feature.

A. noted above, meroaomes, pyenogonids. and arachnids alio have a limb in this position. Kit that does not make them crestactooocpbs. la arthropods, all segments generally carry limfc-t, at least on the head and thorn, it >, only wheo limbs are particularly specialised, or even missing, that things become more interesting and can serve to help diagnose .1 group. For exam pie, the presence of a limb on this first somite posterior to the antennae in crustaceomorphs standi in contrast to what occurs in myriapoJs and insects. In these l itter groups, the limb buds on the first postantennal somite are diverted from forming a limb into producing the Special labrum seen in these groups. We know this is so because, at least foi insects, developmental gene expression studies reveal that the labium Is the "appendage" of thr so called intercalary (firvt postantennal) segment (Boyan et al ;oos).This diversion of the first postantennal anlagen into forming the upper rather than a wtc/liobs dearly is a derived friture It nthelackofhnsbt on the fim postantenaai segment of m^cts and mynapoii duru a noteworthy and significant jporoorphy, not the mere presence of a limb on that segment as otC urs in crustaceomorphs, cheliceriforms, and many fossil groups such as tnlobites.

Crustacea are generally said to have a five-segment head. However, many crustaceomorph groupi iiulude at least one pair of maxilliprds and the associated "thoracic" somite into the head, and we thus speak of a cephateihowx. Most of the time, it it clear that these maxillipcds are obviously modified anterior thoracis limbs. Development in the many crustaccomorph groups that have maxillipcds allows us to document successive stages wherein the maxillipeds become specialised and their associated somiT'i r-rough succeed* main become incorporated into the cephalon dunng ontogeny, Howrcx. at feast ocse group of cnutaceomorpht, the remipedes. does not exhibit such a transition. Koenemaon et aL (;oo~. 1009) observed no biraroous precur- sor stair totheuniramousmaxilliped in the earliest larval stage 1—theremipede maxillipedand its segment are part of the heod in the earliest recognized ontogenetic stages. Consequently, we could »sy that the rcmipede.s, for all intents and purposes, have a six-segment head (Koenemann et al. J009).

In summary, this first part of the diagnosis of Crustacea (head of five somites, each bearing a set of appendages consisting of tv.,» pairs of antennae, a pair of mandibles, and two pairs of nunlUr) a not informative.

"Body consisting of three regions: head, thorax, and 'abdomen"

Body tagmosis is often an important • omponent of defining an arthropod body plan, hot exam- ple. as noted above, among the chelicrrates a discrete head is lacking because the anterior seg mcnls associated with leedirig anil ki-ns

The pom mo" of a head, thorax, ami abdomen is certainly dist inctive. bul it nalso a feature shared with insects. Hence, while we might appear to have, with tagmosas, another argument foe seeking soeae kind of relanoosiup between crustaceomoephi and insects, that a. -

Furthermore, cmstaceomorphs them selves vary considerably in this regard, as we will pur- sue in more detail below. The number of thoracic segments can be characteristic, but only for individual rrmtaceomorphs and not for Crustacea at a whole. Kemipedes have a long, bomonomously developed trunk with no differentiation between anterior and posterior sec- tors. Mntaco. JI hare £re aad branchuraas hare four thoocomeres. Large-bodied bear, chiopods often hair nor iathoracom»r

Moreover, the possession of an alidomei is not a uniting feature. This variability 1* true not only regarding external, gross anatomical features such as total numbers of segments and those with and without paired limbs 00 the segments, but also for the underlying expression of Hox (homeoboi) family gene* as well (Fig. 1.4). In connection with the latter, Abxhanor and Kaufman (1004) and Schram and Koenenaaoa (;«©4») surveyed the available mfonnation concerning Ho* gene expression in crustaceans. There are two fundamentally different types of posterior tagmata: the abdomen, a region without expression of the abd-A (abdominal A) Hox gene; and the pleon, a region with the expression of abd-A Species with the latter type, the malacostracans. possess appendages on the segments and also display a well-differentiated central nervous system in that body rc-gun, whereas species with the former type, which lack abd-A expression ,n that body region (bropods and maxillopodans), lack appendages on these segments aad do 00* have a well-differentiated central nervous system In these segments. It is for this reason that Schram and Koencmann (1004a) concluded that the old term piton, as applied to the posterior region of the trunk of malacostracans. is not just an equal and inter- changeable alt, • native for the term aMo'"'n; the use ol pleon as.i ilcicnptor is an absolute neces- sity. Hox gene expression indicates that the pleon of malacostracans and the abdomen of other crustaceans exhibit fundamentally different developmental pathways

Admittedly, the amount of available data is limited. As it the case with developmental wort, researchers focus on the stedy and manipulation of model oeganiuc*. Among malacostracans. Porccliio Kuf*' and Pracambarui (larln provided the model systems of preference foe Studies of Hox patterning, and among entomostracans, Arteima franciiiana and Mtsocyclopi edax have served as the modeLs, and the latter has been only incompletely investigated. The determina lion of Hox gene expression in diverse arthropods was a leading line of research in arthiupod evo-devo studies in the late 1990s and early 1000s, but such investigations have waned, at least for now. In light of the above phylogenetic usefulness of th:s line of research, we should look forward to moie animals bring investigated in this regard.

NerertheJe... tho part of the defio«>ce c< crustaceans (body ceosatiog of three regions: head, thorax, and "abdomen") is not a particularly informative statement.

"Trunk appendages primitively multiramous"

This descriptor Is also not very informative. The presence of bl- and/or multiramous limbs is widely accepted to be a primitive condition In Arthropoda; mow authorities would concede thai on iramy is derived. Ho»*rer, hew. too, the deed B m the details. Schian and Koeneraanr (:ooi) reviewed the information available concerning early development of crustacean limbs, and Williams (lee chapter j) delves into this subject more deeply. Crustacean Biodiversity and Oisoanty of Socy 'lata

Prac—darkli (Malacostraca)

(Maxiliopoda)

fig-1.4. H

We can summarize here, nevertheless, a lew basic patterns of limb development. One, in which the proximal pedestal of the limb camri dlsully a tubular, segmented telopod, is sometimes referred to as the Drowphila model because it was first recognized and studied in detail using the fruit fly D»ow»pfciJfl (Cohen i«»o). It Is the most common pattern of limb development seen :n all biramous crostainn limbs that have been examined, particularly using Mjudopsis behia (Panganiban et a!, i«w<). The limb anlage becomes forked, leading 15functiona l Morphology and Diversity

eventually to the exopodal and endopodal rami. The gcncdistalless (di/) U expressed at the tips of the developing rami. A rather different pattern, however, prevails in Rranchiopoda, often referred to as the Arlemia model and documented with studies on Anemia and T/iops (Williams and Muller 1996, Williams 1998). Rather than a uni or biramous limb anlage, limb development begins with a mediolatcrally directed ridge upon which eight lobes sub- sequently appear. The expression of dJ7 occurs in varying patterns on these eight lobes, which proceed to form the unarticulated, leaflike limb, or corm, characteristic of the bran- chiopods. Similar gross anatomical sequences of limb development (though without the related gene expression patterns) have been documented for Cydeslheria (Olesen 1999) and the cladocerans (Olesen 1998). Hence, the multiramous limb of branchiopods has a fundamentally different mode of development from that seen in the crustaceans bearing biramous oruniramous limbs.

Thus, this part of the definition of Crustacea (trunk appendages primitively multiramous) is not an informative statement. The statement equates all crustaceomorph limbs and ignores widely divergent, perhaps incompatible, modes of development.

"Development consisting of a series of discrete larval and/or juvenile stages, initiated by a stage termed a nauplius"

In examining this characteristic sequence, we possibly come upon firmer ground in seeking a unique set of features to define Crustacea. Manylivinggroupsofarthropodsexhibitepimorphic development. The animals essentially hatch with the complete set of segments characteristic of the adult, the individuals increase in size only with each molt.

Other groups of arthropods (some of the myriapods), although they resemble the adults in general form, hatch with fewer segments than the adults and add segments with each moll. Some Crustacea do this; for example, pcracarids brood their young, and some of these are expelled from the marsupium as little ")uvenile" forms, called manias, which eventually molt and add a segment to achieve the adult condition.

Many crustaccoinorphs, however, hatch as larvae, and these larvae not only posses fewer segments than the adults but also exhibit a distinctive larval form. Successive molts then not only add segments but also metamorphose the form. Does this constitute an apomorphy for Ctustacea? Other arthropods have larvae Extensive larval stages are known for the trilobites, and pycnogonids have a larva; many larvae, both naupln and Other intriguing forms, are known from the fossil record (see Muller and Walossek 1986). However, there arc distinctive patterns of molting and metamorphosis that serve to absolutely unite some crustaceomorphs. Taxa within Cirripedia arc clearly united by the presence a: a distinctive nauplius with frontola- teral horns and a postnaupliar cypris larva in the life cycle. Branchiopods have a characteris- tic nauplius with a nauplsar process on the antennae. Zocae are diagnostic larvae of decapod malacostracans.

The nauplius Stage is often said to represent a phylotypic stage through which in theory all Crustacea passed in the course of the evolution of the group. We need to express some caution here not all crustaceomorphs begin independent life as a nauplius larva, that is, exhibiting a larva characterised by possession of only three sets of limbs: the first and sec- ond antennae and the mandibles. There are crustaceomorphs that do (or did) not begin life as a nauplius but rather have as the initial Stage a metanauplius, that is, a stage with more than just the three sets of naupliar limbs and/or more than the three naupliar segments. The issue is confused in the literature with the almost completely interchangeable use of the terms naupi'ius and metanauplius Thisinterchangeability implies that it is almost irrel- evant as to what the basic structure of the first larva is—if it LS tiny, possesses only a small number of limbs and segments, is given to swimming, and may or may not be filter feeding. Crustacean Biodiversity and Disparity of Body Plans 16

then it is a "nauplras." We see here the difference between a structural and a lunctional definition.

Which groups have an ortlicmauplius—a larva with only three paits of appendages as seen in Branchiopoda, Mavillopoda. Remipedia, and euphausiacean and dendrobranchiatc

Malacostraca? Each of these orthooaupln bean a distinctive focra. As noted above, branchio- pod nacpUi possess a lUuplar process on the second antenna designed to facilitate feeding.

Variations occar within the MaxiHopoda. Amcng the most distinctive at nauphi, those 01 cirri pedes bear anterolateral boots, frontal filaments anterioe to the first antennae, and a long caudal process. There are four to ax naupliar stages, depending on the group. Copcpod naupiii

exhibit a nauplius in almost incomplete and pristine stJte. although the two oethoiuupliar stages

ate nonfeeding because the gut is not developed um il the metanaupliar phase. Ottracodcs pass

through a single nwiplIUS stage, but the limbs are not completely developed, and in some species

the early developmental stages (nauplius and the metanauplii) are retained within th* mother's

shell until they are shed near the cad of their development. The Cambrian fossil RehlwnidLs

had an ortboaaupliui Finally, the free nanplii of the euphausiaceaas (two) and drrsdrobranchi-

ates (ooc) are very umple m form aad do not feed, and even the socceeding metaruu^ii can he

nonfeeding, also true of remipedrs. Most of the other eumalacostracans pass through a dear

egg-oauplius phase within the egg (Schram 19S6).

The diversity of naupliar form and function led 5cholt 1 (1000) to suggest thai we should dis-

tinguish between primary and secondary nauplu, that is, between naupiii that are Indeed primi-

tive and an original part of the life cycle, and naupiii that are secondarily rccvolved. Scholu.

believes that the primitive stage for malacostracans 11 the cmbryonifed egg nauplius and that

the nonfeeding, free naupiii of eupfcausiaceaiis and dendrobranchiates actually evolved from

ontogenetic sequences without a free nauplius. One consequence of Scholtj s observations is

Other groups of cruttaceomorphs exhibit a variety of first stages in their development.

Cephalocarida begin as a metanaoplius, the first sta^e of which has five limbs and a variable

number of limbless segments. Mystacoiaiida hatch as metanauplii w,th four sets of limbs and

free additional limbless segments.

The significance of ihese metanaupliar stages becomes evident when we consider the lar-

val development in certain of the Cambrian Orsten iiucroartbropods. The larval sequences fot

many of the Cambrian OrMen taxa are known; B'tdecaru. Martinsaonia, and Phosphatocopina

all had four sets of limbs in the earliest phases, what Walossek has referred to at a "head larva"

(Walossefc and Muller Af»oCtu and the othrt tnlobdes in ibea earliest flairs also bear

four. There seems to be a basis for concluding th-t tKe ruupliar stage, with its three let t oflirobs,

is derived from forms with four (possibly five) sets oflimbs.

Larvae are features of aquatic arthropods, but the nauplius larva is undoubtedly a derived

focal. Unfortunately, not all crustaceomorphs have a nauplius, which n perhaps a problem

whose full implication remains to be determined,-some groups may have lost it. but other groups

probably never liaid it

A: the beginning of this section 1 asked the question. What is Crustacea? It appears that

we cannot ate an unambiguous set of apomorphu descriptors to dugnos* a monophyletic

Crustacea. Developmental patterns and the rtaupJuti larra appear to a&a the best chance of

doing >0. However, since we have crustaceomorphs that do not exhibit the naupliar stage, we

might conclude that th* nauplius has evolved .ndcpendently several times in the evolution of

crusttccomcrpht or has been lost several times; otherwise, if one demands that the nauplius be

treated as diagnostic, Crustacea is not a monophyletic group.

It would appear from the above discussion tli«l we must conclude that cruttaccomorphs

are whatever is left over jmong the arthropods after we have assigned everything else to other

dearly defined monophyletic groups. 16 functional Morphology and Diversity

WHAT ARE THE CRUSTACEOMORPH BODY PLANS THAT MIGHT BE MONOPHYLETIC?

We now have a conundrum. If we cannot define a monophyletic Crustacea w ith a single, consist- ent set of derived characters, can we perhaps diagnose smaller mnaophykU. groups within the current array o* cru»taceomorph»> I do believe that there are groups with in this assemblage that are monophyletic (Schram and Koenemann 1004a).

Short-Bodied Forms (Oligo-Crustacea)

Bfanchiura

Two groups of short-bod»ed forms at fust glance would not appear to be at all alike (Fig. 1.4) but share a similarity regarding gonopore location. The living branchiurans are parasites of fish with highly modified mouthparts, hut their gonopores open on the fourth thoracic somite While tliere appears to be an abdomen, it is not differentiated into segments and u little more than a single or bilnbed sac (Fig. i.cA-C). Ot'special note U Pentastomida. the uster group of the branchiurans. Comparative sperm uknstructure (WingHrand i»7s) and molecular sequence studies (Abeie et al. 19*9) revealed a close link of Branchiura with Pentastomida. odd wormlike parasites of the respiratory system in higher vertebrates (Fig i.sK)-

I his pairing of branchiurans and pentastomids might appear peculiar, but It is a group of great age; pentaitomid fossils exist from the eariy Paieoiolc Orsten lauaai (Walossek and Muller 1994, Walotuck et a?. 1994). The leveral species of Cambrian/Ordovxian pentastomids (Fig. 1-sD) can coo. incingly be compared to living [*ntastom»ds (sec Walossek and Muller 1994, their % ai), .hhoufh the fossils hare trunk limbs bat lack the proboscis bearmg the memth. Walossek and cotlcJgues interpret these fossils as parasites, but there is no direct evidence of this. These fossils could have been ordinary free-living members of the infauna. Nevertheless, what the fossils do show without any debate is that, in combination with the sperm a n d sequence data above, the ancestry of branchiurans u very ancient.

Kysraaxo'»dc

In contrast to the l-tanchiurans, the mysL.ocarids are microscopic members of the beach meio- fauna, almost wormhkc in form, with a well-developed set of mouthparts, including maxilli- peds, but with four pairs of rudimentary thoracic limbs (Fig. i.sF). The gonopore. ire loeated on the fourth thorar >c somite. Mystacocarids, too, may be of great age because, in some respects, they are not unlike Skaracarida. the Cambrian fosal group from the Orsten of Sweden (Muller and Walossek (Fig. 1.5G).

Schram and Koenemann (1004a), using morphologic analys.s tempered by Hu« gene cxpres- sion, found mystacoi arids and branchiurans to be sister taxa The results of molecular studies for both of these groups arc confusing be- .use long-branch attraction has been a pei • 1 stent prob- lem in these analyse i; for example. Spears and Abeie (1997) en. ountercd this phenomenon when their results placed mystacocarids, remipedes, and cephatocands together and in some proxim- ity to chelicetatet (» *t ran$e array), aod the branchiurans eroded m a dade w*h podocopan oMracodes. Giribct et al. (*oos) increased both the number of taxa sampled and genes sequenced but obtained a confusing collection of results depending on variant runs of taxa sampled (with •isd without fossils): mystacocarids and branchiurans sometimes appear alongside copepods and .v.tneodes; under other circumstances, branchiurans emerge elsewhere. Although the I a.ion sampling ofCiribet et aL (100$) ^impressive for all arthropods (and especially for he. ipods). it is nut particularly brood within crustaceomorphs. More recently Reg«r et aL (aoo») using nuclear CnrttacMO BioOivttnly and Disparity 0? Body Plans 17

UiU

S. Body cnaxeint IA-C) Dmm [from Scfaram (A)

Aipi*. JCoU bgUy Bo&fxd —*r.«t» »ok tad Uab tepaesaaor.. CD and Q IXyr^nir. totoy (MMMfny« W.M —l M-B., -w,.il«.fi* liX(D)Diagram » tbe Cambr-an gewa Hl7>mw*u tW reduced trcok (0- (E! Dupr rfa (tocrJ- rxcxi l.vmg p«nijgomid. m. mo Cambrian fowl crustacean that might raprucni I iTiyilaLocuid Htm for in. mp. maiillip«

MIIHMKI

Mnillopntti

lfai&iuopodi

RdttpvtKi

few

Kcmlpoili

• MjkciBUi

"jMuilli WOP®

BcutOun Mandibuliti MystKOCinda

.Vihropja. ORracodi

Myrupodi

Chdiccrau • i'yciiugaudi

Ornx KopKon

Fig. (A) A classic undemanding of crustacean pMogenrtic relationships. based on nvorpAology. (BJ A suns- mary version of one ot the mix? recent molecular paylogcuics. Modified a ftci Regirrelil. (JOIO).

piotein coding general so found branchiurantasasistcr|jxoolopodocopanosiracodtaxon sample was again selective; for exam- ple, no mystacocarid was included. To remedy the situation, Regiei et aL (ioio) have expanded the taxon base and increased the number of genes Sequenced; their results identified a clear clade with Mystacocarids. Branchiura, and Pentastomxla within a group they termed "Oligostraca" (Fig. 1.0). The analysis by Koenemann et al. (1010) also placed these short-bodied groups together these short-bodied groups. Oddly, these dades also contained Ostracoda (see below).

The shortness of the body in these orders imposes definite constraints. The lack of an elaborated abdomen in branchiurans and pentastomds undoubtedly limits their ability to move around. One could speculate whether this lack was a factor in both groups adapting para- sitic lifestyles. So, too, with mystacocarids. the lack of a well-developed abdomen could have constrained adapting a vermiform, interstitial existence where abilities to swim or otherwise move around ate minimized.

Branchiopoda thing 8,'anctiiopoda

This large and fascinating group is almost exclusively restricted to freshwater, with a few exceptional cladoeerans that are marine- One is tempted to Speculate that they might have been Crustacean Biodiversity and Disparity of Body Plans 20

manne to begja w*h and then shifted in fresh waters. However, the ndrair foe thai tS not robust. and even most of the fossils, suth a i they are (mosdy cunchostracans), are pre .erred in treshvdter to brackish water situations.

The branchiopods do exhibit a distinctive set of features that outline a body plan for the group. We have noted above in passing the distinctive mode of limb formation—from horizontal ridges that subsequently become multilobed, rather than uni- or biramous limb bud anlagen -and the nauplius larva. Consideration of the large-bodied branchiopods adds some fcrther depth to Mrknowfedge of the braochiopod baaplan, of which Aaostraca serves as a model.

Traditionally (ace Caiman 1909, Schram 1986). anostracans were conceived as having in u-segmcnt thorax and a g-segment abdomen. The first twu legless, abdominal segments formed a fused genital complex. However, Hox gene expression studies reveal that the genes Antennapedia (Anfp), Ultrabithorax (llbt). and abd-A all are expressed in the thorax of Arlcmio, with a resdual expression of A>ep in th» genital segments (FIJ. 1.4). AbdostisaJ 3 (M-B). a marker for "end ot thorax" and the genital segments, occurs in the genital segments (Abrhanov and Kaufman 2004, Schram and Kocnemann 2004a). Hence, the genital segments are better considered thoracic, rather than abdominal, with the gonopores being carried on the twelfth segment of the thorax. The abdominal segments posterior to the genital complex do not exhibit Ho» gene expression.

Notostraca and the conchostracam have the gonoporei opening on the eleventh or between the eleventh and twelfth trunk segments. Notostraca (Fig. carry a -ell-

developed pair of limbs on each of the "thoracic" segments (the first two being somewhat modified from that *een on the others), but posterior to this region the limbs become increasingly smaller as one moves posterior in the sequence of somites, and there is little correspondence between the number ot limbs and the segment boundaries—there are many more limbs than apparent segments. Rrgrrttably, as yet no 1 lox gene expression ttudieshave beeo performed on nntoitracans.

The conchcnsrai. a.u are no* generally divided into three monoph yiefic groups.- Laenca jdau (Fig. 1.7C), Spinii .unlit.1 (Fig. 1.7D), and Cyclestherida (Fig. 1.7E) (Martin and Davis JOOI), but they, too, appear to carry the gonopore in a position similar to that of Notostraca The first of these, the laeviuudauns, or Lynceidae, have fewer trunk Segments than the other twu, but at least the female gonopore opens neai the base of the eleventh, or penultimate, appendage (Under 194 s). The location of the male pore Hill must be confirmed (Martin et al. w«

Thus, most Branchiopoda feature thin, (oliaceous. unfointed limbs, with trunks divided into an anterior section with well developed limbs and good 1 lox expression, and with gonopores at or near the eleventh ot twelfth tmnk somite. The four groups of Qadocera (Fig. I.TI- 1). while they are dearly branchiopods, exhibit extreme forms of body reduction, 01 ocigomery. All these brancfaicpods bear either a well developed carapace or a derivative thereof. Only the aaostra- • "n* (Fig. 1.7J) lack a carapace, and mo*t authorities place the fairy shrimp as a MSter group to all other branchiopods (Bichtcretal. 5007).

The restriction of branchiopods to freshwater habitats entices one to wonder why these groups have bcco.iv-- so limned. The unique mode of limb development perhaps precludes the development of anything other than thin, foliaceous. cormlike appendages. This in turn might have engendered an overall body habitus that lacks weU-sderooted and/or calcified body somites. Under tHr>e constraints, freshwater habitus.especially transient ones, provide satisfac- tory refugia. fonctawul Morphology and Drv^wty

Fig. 1.7. Body H|»» oS Branch lopod a. (A and B) Leptdurm »>i litui, N'oditmca (after Sir) 1U94), with .jrapacc removed (A) »ml ~uh car»p»ce intact (B). (CI) Various conchostracane. (C) Lyrxmi pailharms, Laencattdaa (rnodif-J from Maitm .1 U. v*U\ (D) I•mnad* Iw—WSp^k.^tfata(after Un (E) Cycto*!"«• CycIcthrnda (aftr. San at?). (F-I) Var-x» in(r>order. of CUdoec. (.(tr. lillieboiKiw^Bi.-ge 191*). (F)S*fu

fossil Stein-Sranchiopods

All adhonXi accept crown group Rranchiopoda «s a n***>phy4et»c group, hated on the dis- tinctive nauplius Ian-a and the form and ontogeny of the trunk limbs. However, the branchio pods are also noteworthy in that a number of fossil forms are known that either occupy a stem position to the beanchiopod chde or in some instances actually «tand within the group. Crustacean Biodiversity and Disparity of Body Plans 22

ft- •-»- fmiii species thu outfit iuve some rdjdeoifiip to Brane ftroporf., ei-her near th* taw that group or is SMB lorras. Arrows indicate ih» rwrll'h lhoracoar«TT. the legment at CC |ust posterior to (be rod of i!w thoracic limb set**. -Such aught bear the gonopce*. (A) hfuUtma rW^mux, rvsotuaa (from Scccrtield i9!«). CB> JtehcucA.nlU UmbW*, Upper Cambrian (from Vialossek 1993). (C-E) various Cambrian wapaids. (C.I Ciuj^iawliii ow/a (from Km and /hou 109?). (D) Ptklottrmaaif sptncdomlh

(Irom Taykw 1001). (£) WdflUfitUouis (from DaWi et .1 (F) Orfnuatt' (from Fayers ind Trewin 1003).

The Iipostracan Lrpniocuus ihynlcnsU, a unique Devonian fossil (Fig. i.SA), is preserved in great detail within nodules of chert. The thoiui 11 limbi are both multiramous (thoracopods 1 and 1) and biramous (thoracopods y 0- However, the presence of fully developed maxillae (Schram i9&fl>, rather than the vestigial form characteristic ol true branchiopods. indicates possibly only a sister group relationship with crown Bmnchtopoda. 23 functional Morphology and Diversity

RMttbitli* (Fig, i4B) hit figured prominently m dacraaont of branchiopod origins

(Walossek ivv.l)- However, Schram and Koenemann (JOOI) look exception with thu and con- cluded that Rrhbaihie/la, while possibly a stem form, wa« not a bran.liiopod sensu Mi»cto since not only do they possess bir imuus thoracopods, but also these limbs arise from biramous anla- gen aod nc« the mukilohed r»dge of true beanchiopodt Hence. I believe Rtkkuhj/iij, at bes& Is a stem form.

Another fossil group from the Cambrian could be relevant to understanding stem evolu- tion of branch lopods. the waptuds (Fig 1.8C-E). The genus Waplia from the Burgev-s Shale of

Canada is probably the most famous. However, several genera are known (Beiggt et aL

Chen, and Zhou 1997, Taylor 1001) and all appear to ha*e a subdivide! thorax with apparently four anterior telopodous limbs and Six posterior fohaceous limbs. The gonopores have yet to be identified for waptiids, hut 1 would venture a guess that they probably occurred on the eleventh trunk segment.

Although the recent large scale molecular analyses of Ciribet et al. (aooj) and Wheeler et al.

(1004) typically find Hexapoda as a sitter group to all crustaceomorphs, there is an alterna- tive hypothesis. Schram and Koenemann (1004b), Vanllook and Patel (iOOS), l.arnllot and

Philippe (ioo#), and Dell Ampio et al. (1009) obtained trees with insects and Branchiopoda

eculc sequences, and these trees serve to propose alternative hypotheses concerning branch 10- pod relationships.

Fmaliy, there are fossils such as Cawacollif wiltonae (Fig. 1.8F) that exhibit body plans that are complex but nevertheless place them within branch so?ods. in this case 11 Urge, folia- ceosis, cormlike limbs on the anterior thorax followed by another series of similar limbs but much reduced in sue (Faycrs and Trcwin 1001). Catlncoliis might or might not have had a carapace.

fucrustacea

What remains of the cxustaceomorph ta«a after clades of short-bodied and branchiopo- dan types are isolated is 4 confederation of diverse forms: Cephalocarida. Malacostraca.

Remipedia. and MaxiQopodi. When viewed as a whcvle. these taxa are divergent in teims of both habitus and habitat; nevertheless, oil these groups bear gonopores on the sixth through eighth thoracic somites. There are a couple of interesting exceptions to this rule, which I note below.

CepMocorida

This group of hermaphrodites is small both in sue and In species numbers. It has a thorax of right segment* and a limble»t abdomen of 11 segments (Fig. 1.9A). Thr form of the maxillae is very similar to that seen foi the thoracopoi • The psnopoies are located on the sixth thoracom ere. Nothing U known of Hox gene expression in cephalocarids.

The body plan of cephalocarids might exhibit the results of the same sorts of constraints we saw above with mystacocarids-1 n this case, the elongate, limbless abdomen with extended terminal caudal rami at best probably functions like the tail on a kite: a stabilizer to mini- nine drag and the effect of turbulence as the animals twim. Tbe long series of thoracic limbs developed as .swimmingpaddles provide more locomotory abilities than that seen 111 the tiny thoracopods of mystacocarids, but nsmetheless, competition from larger and more mobile forms probably forced the ccphalocandt to retrea: to floccokm bottom lediments m order to make a living. Crustacean Biodiversity and Disparity of Body Plans 24

TV few a>tet poeft 1=005 the toee tunpUa efOntuera goewpjnr-t'ear.ogsegmrnaiacxaied i>yirn>-? (A) Acephalocarid. HarcbnionefU ™ a. m..««ika,. hermaphrodite with poreon iti»s»lii iho- racomere (modified (roc Schram 14M). (B) A hoplocand MaUeostraca. a male The male pore (tcog im~) would b. 00 the ejhth iho-KWim, the f«m.I. pore (dMCt arrow) ~o«ld be on the sixth thoncomerc (modilied from Caiman 1409). The »yni irid Ana yiifei Mimnfuir. The m-ile pore is on the eighth tfco ncomere ("ong arrow); ihr female pore. 00 sixth thoenoenrre (short an ox) (modified from Schminke ig?A). (F. and F) Two types of remipede. hirmapluodilci with ihr m.l. p.«« on ihe eighth thorxomerr (long arrow) and the fenult pore on the fift.inili the- h nmm (short arrow). (E) Med>um-length fcody. Spr/tOMfll gircmnU (modified from Yafier I«I) (F) Shorl Irnglh body. MiDvpKtC'yugerue (modified from limcrsoo and Schtaro 1991). (G) A typical maxiUopodin, CaUnui /tnnninJucui. Male aDd female pores open on seventh thoracomere (modified from Calniin 1909). 25 functional Morphology and Diversity

Motocosttoca

This most variable of crustacean groups nevertheless has a fundamentally uniform structural plan. The trunk is divided into an anterior thorax of eight segment!, and a posterior pleon of six or seven segments, sometimes fewer. All trunk somites generally bear appendages, but note- worthy variations can occur, such as one or more thoracopods serving as maxillipeds or pos- terior thoracopods and/or pleopods being greatly reduced or absent. Hox genes are expressed throughout the body (Abzhanovand Kaufman 1004. Schram and Koenemann 1004a) with Ubx characteristic of the thorax and abd-A of the pleon (Fig, 1.4). The female gonopores occur in association with the sixth thoracic segment, while the male pores are on the eighth.

The malacostracans .ue typically said to contain three groups: the small nectobenthic icpto- sltacans (not illustrated), the obligate carnivorous hoplocaridans (Fig. 1.9B), and the extremely diverse candoad eumalacostracans that haw forms both with a carapace (Fig. 1.9C) and with- out (Fig. 1-9D). The diversity of this group is examined in greater detail in other chapters in this volume.

We might say that the great versatility imparted by the malacostracan body plan is respon- sible foi its success. The long series of limbs, extending through both the thorax and pleon. allows a great degree of variation and specialization that undoubtedly has allowed the gtoup to radiate to the extent it has, with great numbers of species and remarkable variations in strjeture.

Maxfflopoda

With the problematic Mystacocanda and Braochiura removed from the maxillopodans, where textbooks often place them, there remains a core set ol taxa that appear to conform to a single body plan. The old formula of 5 '< -$ or the newer viewpoint of 5-7-4—five cephalic, seven tho- racic, and four abdominal Somites (see Newman 1987) has great consistency throughout the group. The old interpretation was of a thorax with Six limb-bearing segments and an abdomen of five segments always lacking limbs. An alternative interpretation of the gonopore-bearing segment as actually part of the thorax (Newman 1987) leaves only four abdominal somites: this interpretation makes more sense not only :r. terms of what we can see in other groups, for exam- ple, the free gonopore-bcaring segment of the anostracans that occurs just posterior to a set of trunk limbs mentioned above, but also in termsofwh.it limited information we have concerning I lox gene expression, with Ubx 3nd Abd-A expression in the thorax and abd-B in the genital seg menl (Avetol and I'atel 1997)-

Copepoda (Fig. 1.9G) most clearly present the pattern of 5-7-4. The gonopores of both sexes occur on the seventh thoracomere. Thecostraca conform to the basic matillopodan pat- tern With some variations. Ascothoracica exhibit .s-7-4- Facetotecta appear to manifest 5-7-3. based on the anatomy of the Y-cypris. Ciiripedia exhibit S-7-o, considering the cypris larva as a stand-in model lor the highly derived adults. While male gonopores in the cirripeces appear on the seventh thoracic segment, the female pore has shifted forward onto the first thoracic seg- ment. Furthermore, the ci rnpedes lackan abdomen and coincidently also lack any expression of Abd-A (Mouchcl-Vielh et al. i«S).

The parasitic Tantulocarida present problems since these microscopic forms have an extremely aberrant life cycle. However, recent advances in elucidating that life cycle (Huys et al. I9) allow us to conclude that the tantulocarids express a 5-7-2 pattern, with the male gonopore appearing on the seventh thoracic somite and the single median female pore occurring on the first. This latter feature clearly unites tantulocarids and thecostracans as sister groups. Crustacean Biodiversity and Disparity of Body Plans 26

The constraint* exerted by a limbless abdomen on lifestyle may explain much of what wc sec in maxillopodan evolution. The maxillopodans certainly thrive under unusual conditions. Parasitism is widespread in the group, especially among thecostracans, and those thecostracans that arc not parasites have lost the abdomen altogether and settled (literally) into the completely sedentary, highly aberrant body plan seen in the barnacles. Only the copepods possess the kind of biodiversity and habitat variability we associate with "successful" groups. Even so, the small SIMS of copepods could be related to the limits engendered by an abdomen lacking limbs.

Qstrocoda

These animals remain the most vexing of arthropods to place phyloger.etically and, if molecular sequences are to be believed, may not be a monophyletic group Thei r extreme reduction ofbody plan (oligomrry), complete enclosure within a calcareous shell, and specializations directed at life carried on at a microscale have hindered attempts to link them to other crustaceomorphs. There are contentious debates about homologies within Ostracoda (Home et aL 200s). and ostracodcs do not appear to share obvious apomocphics with other crustaceomorphs. Most textbooks and reference books consign ostracodcs to the ma.«illopo>l.iivs (see Schram 1986), but tliat is more of a default placement.

K. Martens (personal communication, Z004) and R.A. Jcnncr (personal communication, i009) expressed an informal view of at least some researchers that Ostracoda might noe be a monophyletic group. This possibility obtains some support from molccular data that some- times finds Podocopa and Myodocopa in different pans of cladograrr.s (see Spears and Abele 1997, Regier et al. 2008. 2010, Koenemanil Ct al. 2010). I lowever, most of these, analyses have a very limited taxon sample with sequences from only a handful ofostracodc species.

There is much variation in form in ostracode limbs, but there is a consensusat least that both the myodocopcs aod the podocoper. are themselves monophyletic (I lorne et al. 2005). However, debates about the number of somites in each group are not settled. At first glance, one perceives that only very few thoracic segments bear limbs, but Sdiulz (1976) presented some evidence thar indicates CyihtrcUa port, a podocopan, might have 11 trunk somites (a S-7-t pattern) and that the penis appeats to be associated with the sixth or seventh of these segments (see Schram 19S6, their fig. j}-iC). Tsukagoshi and Parker (aooo) confirmed this in other species of podocopans. No similar information is available yet for Myodocopa.

From this, it might appear that podocopan ostracodcs are possibly maxillopodans. Some authorities classified Ostracoda as a subclass of Maxillopoda (Schram 1980), but others main- tain them as an independent class (Martin and Davis 2001). Most recently, Kocnemann ct al. (2010) and Regier Ct al. (1010), or. the basis of molccular sequences, obtained both podocopan and myodocopan ostracodes as a sister group to a clade of mystacocarids, branchiurans, and pentastomidf. This arrangement would then unite all the short-bodied "oligostracans" into a Single clade near the base of the crustaccomorph tree (fig. 1 A).

1 lowever, there existed Pa leojoic, especially Cambrian, taxa that may have some bearing on eventually determining ostracode affinities. Several such groups arc under active study, such as the luadoiiids, Phosphatocopida (Maas et al. aooj), and perhaps even the thyUcoccplulans. These groups will eventually have to be integrated into any classification of the crustaceo- morphs, and undoubtedly they will prove very interesting in this regard.

Remipedta

This most recently discovered group of crustaceomorphs is noteworthy for several rea sons. The trunk is not differentiated into a thorax and abdomen/'pleon. If we consider the 27functiona l Morphology and Diversity

maxilliped-b earing segment as a modified trunk somite (even though it is completely merged into the ccphakm). then the female gonopore occurs on the eighth postmaxillary segment, and the male gonopore, on the fifteenth. However, as noted above (Koenemann et al. 4007. 2009). the distinctive ma»iliipeds, virtually identical in genera! form to the maxillae, display nodes-cl- op mental evidence that thislimb is modified from a thoracopod format. In addition, the number a: trunk segments is not fixed, either w.thin or between species (Koenemann et al. 1006), with many long-bodied forms recognized (Fig. 1.9E)—although there appears to be at least a lower limit of 16 trunk segments in the adults (Fig. 1.9F). The significance ofall th is variability remains to be explored.

The reraipede body plan ensured that these animals are excellent swimmers, on a par w,th anything seen among the malacostracans. liven so, their habitat restrictions are quite profound; they prefer anchialine cave habstats in low-oxygen condition s.

CLASSIFICATION

The above review indicates there have to be changes in our concepts of crustaccomorph classification, but this is not the place to present any new 01 radical higher taxonomy. In pnnci pie. we want our taxonomies to reflect phytogeny, but that is not always possible. There is much conflicting evidence from molecular analyses, which along with morphological data often suf- fers from limited taxon sampling, and the latter often ignores or minimises input from fossils. We still need to more effectively integrate data from gross morphology, molecular sequencing, and paleontology into a coherent whole. Nevertheless, we should extend some effort to rec- ognize the monophyletic groups about which we are certain (Fig. 1.10); there are patterns that should be acknowledged.

To these ends, wc can make good use of the concept of the pletlon, a particular taxon that docs not fit well into another category and that eventually m ight be assigned to its own higher category. I believe that, in this instance, wc should begin to think of (be infraphyia below as monophyletic groups on a par with other well-established arthropod monophyla such as Hexapoda, Chclicerata. Trilobita, and Pycnogonida. What fossils and where thev will fall within or between these monophyletic groups will be explored elsewhere. The scheme is not complete in tetms ofall possible fossil plesions but docs include most of those mentioned in the text above (Table 1.4).

WHAT MIGHT THE CRUSTACEOMORPH ANCESTOR HAVE LOOKED LIKE?

At one time, there wis a lair consensus as to what the ancestor of Crustacea might have looked like. Hessici and Newman (1975) devised an ancestor with a long, homonomously segmented body, each segment bearing a set of li mbs not unlike a cephalocarid, for which Newman preferred a form with a carapace, and Hcssler one without (Fig. i.ilA). Cisne (19S1) believed that crusta- ceans arose from a Irilubite-Iike ancestor. Schram (198:) concurred with HessJer and Newman ('9?.<)> although he weak: haveprcferred a somewhat more foi iaceous limb, intermediate between cephalocarids and brancbiopods (Fig. 1.11B). However, Schram s 1981 paper had been written in 197S (delayed due to a delay in the publication of the book in which it appeared), and in the inter- vening years the rem,pedes had come to light. By 1981, Schram had altered his views as to the form of an ancestor, which, while Still in possession of a long homonomous body, was viewed as equipped with biramous, paddlelikc limhs (Schram 1984). Schram positioned this biramous theory as an alternative hypothesis to the inixopodial theory of Hessler and Newman, and this then postulated a rcmipcde-like alternative ancestor as opposed to accphalocarid-like forebear. Crustacean Biodiversity and Disparity of Body Plans 28

VCrMnns- Mntacocandi fr-S T JDb- Minllopodi

Milaoona

•iimivim^ Rnnipoii

U

J. J J khhMMWV Pop.hiopoj,

Mayorcrustactonwrph body plans based on Ror-opore pontion. (A) Mystacociridi, in "obgostracin." (B) "EoCtuSUCCiiSS." (C) Branchiopcda. From Schram and Kotncminn (ioo«i).

The debate outlined above wis based on morphology. Some information derived from molccular sequences now suggests that hexapods could factor into this mi*. One fossil that might have facilitated a visual understanding of how this transition might have occurred is IVingrrtscfceliiciiS bflkeii Briggs and Battels, 2001 (- Dtvonohcxapodus bockibergcnsii Haas ct al., 200}). A recent reexamination of all available fossils of this species from the famous Devonian Hunsrucfc Shale (Kuhl and Rust 2009) synonymu.ed the two names, but the origi- nal reconstruction of Haas Ct al. (1003) presented a strange chimera—it appears to have a dragonfly anterior end and a very long myriapodous posterior end (Fig. x.iiC). Although the interpretation of Haas et al. (»00j) of D. bodcibergeniis offered a head (of possibly foursegments) and a short three-segment thorax followed by a long abdomen, the new interpretation presents a six or seven-segment head, with the postenormost three pairs of cephalic limbs as long, pos- sibly prehensile appendages and followed by a long trunk with biramous limbs. Neither Briggs and Battels (2001) nor Kuhl and Rust (:

Another source of information that is relevant for understanding crustacean ancestry is deris-ed from the study of the Cambrian Orsten microfossils (a few of which were mentioned 29functiona l Morphology and Diversity

".'I » ' •. A classification of tetraconate arthropods with inclusion of fossil plesions.

Subphylura:Tetf»COoata(-Ciusuccomorpha - Pancrustacea) Infraphylum. Hexapoda

Infiaphyhim- unnamed (shoit-bodied crustaceomorphs—"Ohgostraca") Class Branchiura Order: A rguloida Order: i'entastomida Class: Mysucocanda Plesion: Skaracarida

Plesion- Ostracoda (one possible position; includes Myodocopa and Podocopa) Infraphylum: Branchxtpoda

Class: Phvllopoda (- Calmanostiaca) Order: Lacvicaudata Order: Notostraca Order. Spinicaudata Older CycleStherida Order: (lladocera CUss: Sarsosiraca

Order: Anostraca Plesion- Lipostraca (- L(put/tos) Plesion: Rchbachirllida (= RekbaefiitlUi) Plesion: Waptiidae Infraphylum: Crustacea Class: Cepbak>ca:idu Class: Maxillopoda Subclass: Copepoda Subclass. Thecossraca Infraclass: Ascothoracica InfracliSS: Cirripedia Infraclass: Facetotecta lofraclass: Tantulocarida Plesion: Ostracoda (one possible position; includes Myodocopa and Podocopa) Class: Malacostraca

Subclass. Humalacostraca Subclass: Hoplocarida Subclass: Phyllocarida Class: Remipedia

(>lililxati-li "i>! Krmipcdiiaiipi (CIIWKN-H'diss,Xciomii).SJKScimotiulunidimr.OnuwlKDaU oreiW r-x- pwiitfr poilGoos- anaos otgovnaa*, o» or firhin iHiillopidios, bised «i tcrnr ffArfjin^s^itiiii llrtjv'tf ra.*ltl> in.*: (•cniabta) vnlki{rijnoCuuljJi xz

above), and these have raised the possibility ol alternative hypotheses. Incompletely under- stood in the i>;5os, the depth ol knowledge about these animals is now astounding, extend ing as it docs to even developmental stages for many of these species (see chapter a). The full impact of these studies remains to be assessed within the larger framework of the anatomy of modern forms, molecular sequences, and gene expressions, but much of this work suggests a Crustacean Biodiversity and Disparity of Body Plans 30

Fig.I.il. Crustaccomorpb ancestors (m< if it tor dcnils). (A and A") Without and with a carapace. according to llciilo' and Newman (197S)• (B) According to Schnm (hiSj). (C) tV«we*«*-ibetktktrgcmii (from llaa.ictal.aoa>}.

possible alternative hypothesis: a short-b«xiicd ancestor rather than a long-bodied one. This merits consideration (Schram and Kaenemar.n 2004a). but it is not possible or appropriate to examine here.

CONCLUSIONS

It would appear that we arc little closer to understanding the origin ofcrustaceomorphs than wc were 30 years ago. While the larger assemblage of the crustaceomorphs (or pancrnstaceans, or letraconotans, if you prefer) might be in some way monophyletic, just how it can (or es-en if it can) be diagnosed with a single set of apomorphies is not clear at this point. There arc, how- ever, good monophylctic groups within this vast array that can be dearly defined. Furthermore, these body plans appear to be constrained regarding biodiversity, functional morphology, and habitats they can occupy. 1 n add ition, we have a growing array of fascinating fossil taxa scattered within and between these monophyla, but how these ate related to the monophyletic groups for which they may serve as stem forms remains to be determined.

But take heart! It is a time not to mourn the demise of the monophylum Crustacea but to embrace what will be a new woiid order and a better understanding of this whole branch of the crastaceomorph arthropods.

ACKNOWLEDGMENTS

I am grateful for the invitation fiom Profs. Martin Thiel and I.cs Watling to write this chap- ter. 1 also think Or. Ronald Jenner (Natural History Museum, London) for reading a draft and offering some valuable comments and suggestions. Prof. Stefan Koenemann (Hannover) was involved in producing some of the earlier papers from which parts of this chapter developed. Any and all faults, however, a rc my own. 31functiona l Morphology and Diversity

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