Neurobiology of the Anomura: Paguroidea, Galatheoidea and Hippoidea

9 Pages·2003·7.2 MB·English

by  D H Paul

MemoirsofMuseumVictoria60(1):3-11 (2003)
ISSN 1447-2546(Print) 1447-2554(On-line)
http://www.museum.vic.gov.au/memoirs
Neurobiology ofthe Anomura: Paguroidea, Galatheoidea and Hippoidea
DorothyHaymanPaul
DepartmentofBiology,UniversityofVictoria,Box3020,Victoria,BCV8W3N5,Canada([email protected])
Abstract Paul,D.H.2003.NeurobiologyoftheAnomura:Paguroidea,GalatheoideaandHippoidea.In:Lemaitre,R.,andTudge,
C.C. (eds). Biology ofthe Anomura. Proceedings of a symposium at the Fifth International Cmstacean Congress,
Melbourne,Australia,9-13July2001.MemoirsofMuseumVictoria60(1):3-11.
Anomuransarevaluablesubjectsforneurobiologicalinvestigationsbecauseoftheirdiversebodyformsandbehav-
iours.Comparativeanalysesofpostureandlocomotioninmembersofdifferentfamiliesrevealthatperipheraldifferences
(in skeleton andmusculature) account formuch ofthebehavioural differences between hermitcrabs andmacrurans
(crayfish),squatlobstersandcrayfish,hippoidsandcrabsandsquatlobsters, andalbuneidandhippidsandcrabs,and
thattherearecorrelateddifferencesinthecentralnervoussystems.Theorderofevolutionarychangeindiscreteneural
characterscanbereconstructedbymappingthemontoaphylogenyobtainedfromotherkindsofdata,suchasmolecu-
larandmorphological.Suchneuralphylogeniesprovideinformationaboutthewaysinwhichneuralevolutionhasoper-
ated.Theyarealsousefulindevelopinghypothesesaboutfunctionofspecificneuralelementsinindividualspeciesthat
wouldnotbeforthcomingfromresearchonsinglespeciesalone.Finally,comparativeneurobiologicaldataconstitutea
largelyuntappedreservoirofinformationaboutanomuranbiology andanomuranrelationshipsthat, asmorebecomes
available,maybehelpfulinsystematicsandphylogenetics.
Keywords Cmstacea,Anomura,neurobiology
Introduction speciation?Wearefarfromachievingdefinitiveanswerstoany
ofthesequestions,particularlythelastone,butthecomparative
Thediversityofbodyformsandbehavioursthathaveevolved dataontheneurobiologyofsomeanomuranssummarizedhere
within the Anomura (Fig. 1) offer neurobiologists numerous indicatethedirectiontowardwhichtheanswersarelikelytolie.
opportunitiestoexaminevariantsinformandfunctioniniden- Fromanentirelydifferentperspective,comparativeresearchon
tified neurons and neural circuits mediating specific move-
adultandembryonicnervous systemscanprovidetaxonomists
ments orelements ofbehaviourandtherelationships between
and evolutionary biologists with useful characters to supple-
them. This is because discrete and identifiable neural differ- ment other types of data used to construct phylogenies
ences are expected to underlie inter-specific differences in
(Breidbach and Kutsch, 1995; Harzsch and Waloszek, 2000;
behaviour ranging from single movements of individual
Sandeman and Scholtz, 1995; Scholtz and Richter, 1995;
appendagestoagonisticinteractions.Thevariantsinamplitude
Strausfeld, 1998; Whitington, 1995; Whitington and Bacon,
and order ofpereopodjoint movement during locomotion or
1997).Thisisbecausenervoussystemsarerelativelyconserva-
posturing during socialencounters, orinthe socialbehaviours
tive through evolution (compared with other internal tissues
themselves, may thereforebeviewedas theresults ofnatural,
and organ systems), although not to the degree once thought
as opposed to invasive, experiments to manipulate different
(Whitington, 1995; this review). Species differences between
neurophysiological and neuroanatomical parameters in the
identified neurons and neural connections can be recognized
nervous system ofone taxonomic group (Antonsen and Paul,
because they stand out against a background of highly con-
1997,2000,2002;FaulkesandPaul, 1997b, 1998;Paul, 1991).
servedneuralarchitecture.Mostcomparativeworkhasbeenat
Inadditiontoinvestigatingmechanisticissuesinneuroscience, higher taxonomic levels, and the Anomura, considering their
mseuncthalcoqmupeasrtaitoinvseirneseevaorlcuhticonaanrybengeiunrotboiaodldorgeyssas:suHchowfucnodna-- Ddievcearspiotdya,.are under-represented even in studies focusing on
servative are neurons and neuronal circuits? Are some
morphological and physiological features more easily (i.e., Comparative neurobiological research. Neurons and neuro-
often) modified than others during behavioural evolution? behaviouralcircuits donotfossilize, whichmakesrecognition
Whatconstraints onchanging complexneuronal networks are ofmodernsurrogatesforancestralneuraltraitsessentialforan
imposed by the necessity that they remain functional through understanding of nervous system evolution. In external
4 DorothyHayman Paul
S Munida Galathea Blepharipoda Lipidopa Emerita
quadrispina strigosa occidentalis califomica analoga
FAC
hMoG
Porcellanidae Galatheidae Albuneidae Hippidae
^ nonspikingTUSR
gait4 spikingTUSR
switch leg4~nropod^
nonG^nropod
beating
Galatheoidea Hippoidea Pagnroidea
legs-nonG^
^
walking digging^
fTTTTl hMoG RSM
MoG
spikingTUSR
MG
Thalassinidea Anomura Brachyura
Astacidea
nonG
AT
VTF
lgI
MG,LG,MoG,nonG,FAC,VTF,walking(CPG/leg)
Figure 1.NeuralcharactersandsystemsdiscussedmappedontoapartialphylogenyofReptantia(basedonMorrisonetal.,2001,andSchram,
2001). Filledboxes: characterpresent; hatchedboxes: charactermodified; openboxes: characterlost.AT-anteriortelsonmuscle andmoto-
neuron; FAC -fast, anterior, contralateral flexor motoneurons; hMoG- homologue ofMoG (Sillar and Heitler, 1985); MG-medial giant
interneuronpair;LG-lateralgiantinterneurons;MG-medialgiantintemeurons;“MG”-modifiedMGsystem(HeitlerandFraser,1986,1987);
MoG-motorgiantflexormotoneuron; nonG-non-giant(asopposedto LGs, orMGs) interneuron systemfor swimmingbyrepetitivetail-
flipping; RSM -return stroke muscle and motoneurons; TUSR - telson-uropod stretch receptor (nonspiking: graded potentials transmitted;
spiking:receptorpotentialconvertedtoactionpotentials).VTF-ventraltelsonflexormuscle. 1.Itisdebatedwhetherhomologuesofmacruran
MGandLGneuronshavebeenretainedinbrachyuranthoracicnervecord.RetentionofMGhomologuescouldbeexpectedfortheirdirectcon-
nectionstolegpromotormotoneurons,whichincrayfishcausethelegstoextendforward,thuscontributingtotherearwardtrajectoryoftheMG-
triggeredtailflips(HeitlerandFraser, 1989).TheLGneuronshavenoknownoutputtothoraciclegmusculatureinmacruransandarepresumed
absentfromBrachyura. IfLGhomologues arepresent, thentheirlosses fromthethalassinid and anomuranlineagesoccurredindependently.
2.Thestereotypedmovementsofsandcrabs’(Hippoidea)digginglegsdifferbetweenlegs2/3 andleg4,corresponding,respectively,toback-
wardwalkingandforwardwalkingmovementsinotherspecies(FaulkesandPaul, 1998).3.Rhythmicmovementsofthelegsand“tail”co-occur
inHippoidea,whereastheirhomologues(walkingandtailflipping)inwalkingspeciesaremutuallyexcusive(FaulkesandPaul, 1997a).4.Right
andleftlegsofeachsegmentalternateatonsetofdigging,thenswitchtobilateralsynchrony(FaulkesandPaul, 1997b). 5.Rhythmicdigging
movementsofthefourthlegsarecoordinatedwithuropodstrokes(homologueofnonGflexions)ratherthanwiththeanteriorlegs(Faulkesand
Paul, 1997a). Not included are the changes from the ancestral macmran condition in aminergic systems and agonistic behaviours of
M. quadrispina(AntonsenandPaul, 1997,2001).
NeurobiologyoftheAnomura 5
morphologyandmodesoflocomotion,galatheidsmostclosely and hermit crabs were the first neurons in crustacean central
resemble macruranreptantians, such as crayfish. The external nervous systems to be recognized as re-identifiable neurons
form of crayfish, particularly of the abdomen and tailfan, is (seereferencesinBullockandHorridge, 1965); investigations
similartothatoftheearlyfossildecapodPaleopalaemonnew- oftheirphysiology,inter-connectionswithotherneurons,roles
berryi (Schram et al., 1978). Similar morphology suggests inlocomotion, and, more recently, in agonistic behaviours in
similar behaviour, in this case, posture and uses ofthe “tail”, crayfish continue to inform us about how crustacean behav-
makingneurobiologicaldataon sensory andmotorsystemsin iours are mediated, as well as about general mechanism of
crayfish forthe mostpart suitable surrogates forthe ancestral nervous system function (Edwards et al., 1999; Wine, 1984).
decapod condition. Therefore, regardless of specific phylo- Crayfish’s MG and LG neurons, with associated motor giant
genetic relationships, many neurobiological features of cray- and segmental giantneurons, coordinatethe rapidandpower-
fishes may reasonably be considered surrogates for the fulflexions oftheabdomen-tailfancalledtailflips (Edwardset
ancestral condition of homologous features in anomurans al., 1999;Wine, 1984).Anomuranshavemodified(Paguroidea)
(Paul, 1989a, 1991;Pauletal., 1985,2002). or lost (Galatheoidea, Hippoidea) these giant interneuron
MG
systems(Fig. 1).Onlythe system,includingthesegmental
and motor giant neurons, is retained, with modifications, in
Anomuranneurobiology pagurids to subserve their new mode of escape: rapid with-
Anomurans have, by definition, modified the ancestral mac- drawal into their gastropod shell (Chappie, 1966; Heitler and
ruranreptantian“tail”(abdomenandtailfan).Themostobvious Fs1ri9ao8sn6es)r,in1t9h8e6,pa1g9u8r7i;dUnmerbvaocuhsasnydstLeamngo,fa1c9q8u1i)r.inSgoamehyrderpoesrtcautsi-c
coiTelated neural difference from their macruran ancestors is
skeleton, asymmetricalabdomen, anduseofthelasttwopairs
fusion of the first abdominal with the last thoracic ganglia,
leaving five free abdominal ganglia in the “tail”, the homo- ofpereopodstotransportgastropodshellsforshelterhavebeen
loguesofmacruranabdominalganglia2through6.Thecytoar- investigated (BentandChappie, 1977; Chappie, 1966, 1969a,
chitecture ofabdominal ganglion 1 ingalatheids andhippoids b,c, 197b3u;t19m9a3n;yChianptperieestainndgHqeuaersnteiyo,ns19r7e6m;aiHne,rresiudchandasFutlhle,
hasnotsubstantiallychanged,however,sothatidentificationof ,
homologues of its neurons with those in the more posterior csownitmrmoelroeftst,hewthaeilnfapnr’essegnrti.pTohnetphaertsihaelllreavnedrsoifonthtoetaasiylfmamnestyrmi-c
abdominal ganglia, as well as with neurons in macruran
metry in pagurid species using straight shells (Imafuku and
abdominalganglia,isrelativelystraightforward(Antonsenand
Ando, 1999) has likely engendered some modifications inthe
Paul, 2001a; Mittenthal and Wine, 1978; Wallis et al., 1995;
Wilson and Paul, 1987). Nineteenth and early twentieth muscles andreflexcontrolofthe“tail”fromthoseinpagurids
hoisting spiraled shells (seeChappie, 1966, 1969b, 1973); are
centuryneurobiologists(or,inthevocabularyofthetime,zool- theyreversionstothemacruranconditionornewpermutations
eogsitsitnsg,faenaattuormeissta,bpohuytsicorluosgtiasctesa)n,deisnccrliubdeidngapsloemtheoraanoofmuirntaenr,- oftheasymmetric senMsoGry-motorsystemsofotherpagurids?
T1h98e7)retention ofthe interneurons andrelated circuitry in
behavioursandnervoussystems(seereferencesinBullockand
Horridge, 1965), many ofwhich could profitably be revisited pagurids (also in Thalassinidea: Bullock and Horridge, 1965;
with modern research tools. For example, Alexandrowicz Paul, pers. obs.) illustrates that evolutionarily conserved
neuronal networks can retained the ability to coordinate
(1951, 1952,1954),throughunparalleleduseofmethyleneblue
movements inthe faceofsubstantial alterations inperipheral,
staining, described details of dorsal muscle receptor organs
skeleto-muscularsystems.
(analogues ofmammalianmuscle spindles) innumerous crus- GalatheoideaandHippoideahaveapparentlylostbothMGs
ttraacteiaonnss,fiosntcelrueddinpgiopnaegeurriindgs.elAelcetrxoapnhdyrsoiowliocgzi’csalexwqouriskitoenitlhleusse- andLGs(SillarandHeitler, 1985;Paul, 1991;WilsonandPaul,
sense organs which continues today (Macmillan, 2002; . However, both perform repetitive tailflipping, rapid
MacmillanandPatullo,2001;Pilgrim, 1960). extensions-flexions ofthe “tail”, suchas used by crayfish for
swimming, and which are presumably mediated by homo-
Although most often studied in macruran decapods
loguesofcrayfish’snon-giantcircuitryforswimming(thiscir-
m(uMasccmliellraenc,ept2o0r02)o,rgabnilsat(erMalROp)airasreofpresseegnmtenitnallHyoplaorcraarnigdead cuitryiscallednon-giant,nonG,becauseneitherMGsnorLGs
are involved) (Paul, 1981a, 1991; Sillar and Heitler, 1985;
(Alexandowicz, 1954)andSyncarida(Wallis, 1995)and,there-
Wilson and Paul, 1987). Unexpectedly, the two squat lobster
fore,presumedancestralinMalacostraca.Furtherinvestigation
ofthe MROs thathavebeendescribed ingalatheid squatlob- species thathavebeeninvestigateddifferintheircomplement
offast flexor motoneurons, although their tailflipping behav-
sters (Pilgrim, 1960; Wallis et al., 1994) and pagurid species
(Alexandrowicz, 1952; Pilgrim, 1960, 1974), aswellasinves- iours appear to be indistinguishable (Fig. 1). In Galathea
strigosa, theclusters offastflexormotoneurons are similarto
tigationsinotheranomurans,arecertaintoprovideinsightinto
horogwanesvoclounttiroinbaurtyemtooditfhiecatdiiostnisncitnivtehispoasrtruaryesofaanndciefnotrmssensoef ttahlolsyerienpecartaeyfdismho,toirn-cgliuadnitngmohtoomnoeluorgouness(oFfigc.ra1y,fhisMho’sG)sewghmeinc-h
locomotionintheAnomura(Wallisetal., 1994). helaevcet,richaolwecvoeuprl,inlgosttotthheesgpieacnitaliinzteedrnefeuartounrsesanadssboecciaotmeedmwoirt-h
Motorsystems -fromfamiliarto novelfonns ofposture and phologically similar to other fast flexor motoneurons (Sillar
movement. The paired, dorsal, medial giant (MG) and lateral and Heitler, 1985). Munida quadrispina, by contrast, has not
giant(LG)intemeuronsinthenervecordsofmacruranspecies onlylostmotor-gianthomologuesbutalsotheentireclusterof
6 DorothyHaymanPaul
anterior contralateral fast flexor motoneurons (Wilson and return-stroke muscle in the telson, innervated by three
Paul, 1987). Since no functional or behavioural correlates of motoneurons (two excitatory, one inhibitory), occurs only in
these neural differences are evident, it appears thatevolution- hippoids (Paul et al., 1985); it is very small in albuneids, but
arychangesinnervous systemsduringspeciationoccasionally hasbecomeone ofthelargestmuscles inthebodyofhippids.
occurindependentlyofalteredmorphologyorbehaviour. Such Withoutit, the largereturn stroke movementofthe uropodin
events would leave overtly similar sibling species with hippids wouldbe impossible (Paul, 1981b; Paul et al., 1985).
different potential for subsequentneurobehavioural evolution. This new movement is monitored by a new telson-uropod
Other squat lobsters should be investigated to determine stretchreceptorthatisuniquetohippids.
whetherthesedataarerepresentativeofthesegenera,inwhich
case they would suggest that Mimida is more derived than Novel stretch receptors. Telson-uropod stretch receptors (Fig.
Galathea. 1, TUSR) are found only in squat lobsters (Galatheidae) and
Porcelain crabs (Porcellanidae) flap their small, flat sandcrabs(Hippoidea)(Maitlandetal., 1982;Paul, 1972;Paul
abdomens rhythmically to swim upside down (Hsueh et al., andWilson, 1994;WilsonandPaul, 1990).Theyarecloseand
1998)andtostabilizetheirdescenttothebottomafterdropping approximately parallel to the anteriorTelson-Uropodalis mus-
off vertical surfaces (Paul, pers. obs.). This is presumably a cle (= the hippid Dorso-Medial muscle), which is relatively
reducedformofthevigorous swimmingmovementsexhibited largerthanitshomologueinmacruransandoccupiesthespace
byGalatheidaeandcrayfish,andthereforehomologoustonon- in the anterior telson vacated by the loss of the macruran
giant tailflipping. Nothing is known about the musculature, AnteriorTelsonmuscle(Pauletal., 1985).Thesensoryneurons
motoneurons,orthecentralcircuitryexecutingthisporcellanid oftheTUSRsareunusualbecausetheyaremonopolarandtheir
behaviour, but it is an almost certainty that porcellanids lost somataarelocatedinthelast, sixthabdominal,ganglionofthe
MoG, as have M. quadrispina and the Hippoidea, rather than ventral nerve cord; i.e., theircentral morphology, like that of
transferred them into ordinary fast flexor motoneurons, as similar stretch receptors associated with the macruran swim-
occurredinG. strigosa(hMoGinFig. 1). meretsandmacruranandbrachyuranpereopods,resemblesthat
Non-gianttailflipping was alsoretainedinbothfamilies of ofmotoneurons(Bush, 1976).Typicalmechanosensoryneurons
sandcrabs (Hippoidea;Fig. 1).Inalbuneidspecies,thisisevi- inarthropodsarebi-ormultipolarandtheircellbodieslieout-
dent as the tail-“flapping” they use, along withrowingmove- sidethecentralnervous system,closetotheperiphery.Telson-
ments oftheirpereopods, to swim awkwardly upside down- uropod stretchreceptors apparently evolved twice, first inthe
likeporcelaincrabsdescribedabove-(Paul, 1981a)aswellas galatheoid-hippoid common ancestor and again in hippids.
to assist the pereopods when digging into sand (Faulkes and Alternatively, the first telson-uropod stretch receptor could
Paul, 1997a,b, 1998).Theretentionofnon-gianttailflippingin haveevolvedpriortothepaguroiddivergence andwas subse-
hippid sand crabs is less obvious, because they keep their quentlylostinhermitcrabs.TheTUSRsinGalatheastrigosa,
abdomen flexed beneath them and beat their highly modified Munidaquadrispina,andBlepharipodaoccidentalis(Maitland
uropodsrapidlybothtoswim(Paul 1971, 1981a)andassistthe etal., 1982; Paul andWilson, 1994) andLepidopa californica
pereopods in digging (Faulkes and Paul, 1997a, b, 1998). (Paul,pers.obs.)aremorphologicallyandphysiologicallyvery
Homologies between individual muscles in sand crabs and similar and presumed homologues. The central location and
Otherdecapodspecieshavebeenconfirmedbyexaminationof morphology of their sensory neurons are similar, and these
theirinnervations, specificallythe locations andmorphologies neurons generate conventional action potentials when their
ofthe motoneurons innervating them, which are highly con- peripheral dendrites are stretched by elevation ofthe uropod
served (Paul, 1981b; Paul et al, 1985), but evidence for the (Maitlandetal., 1982;PaulandWilson, 1994).Nocomparable
homology ofhippids’ swimming-by-uropod- beating and tail- proprioceptors monitoring movement ofthe basaljoint ofthe
flipping is indirect but substantial: numerous similarities uropod have been found in any macruran or pagurid, which
betweenmotorpatternsandbetweenhomologousmotoneurons suggeststhatthegreaterfreedomofmovementofthe uropods
activating functionally divergent, homologous muscles (Paul, ingalatheoidsandhippoids (Pauletal., 1985)mayhavemade
1981a, b, 1991; Paul et al., 1985; Fig. 1). Directtests ofthis theevolutionofaproprioceptortomonitorwholelimbmove-
hypothesiswillrequirecomparisonoftheneuronalcircuitsfor mentadvantageous.Theabdomen-propoditechordotonalorgan
thesetwobehaviours, andlittleisknownabouteitherofthem, intheuropodofcrayfishoriginatesfromthethirdnerveofthe
other than that both rely on central pattern generation (Paul, sixthabdominalganglionasthisnerveenterstheuropod(Field
1979;Reichertetal., 1981; seeDiscussion). et al., 1990). Since its proximal attachment is flexible, this
Muchofthedifferenceinformbetweenuropodbeatingand receptorwouldbeunsuitedtomonitoringmovementacrossthe
tailflippingcanbeaccountedforbybiomechanicaldifferences, much more mobile articulation ofthe uropod with segment 6
duetochangesintheuropodarticulationandthetelson-uropod in squat lobsters and sand crabs (Paul et al., 1985), and no
musculatureinhippids(Paul, 1981a,b, 1991;Pauletal., 1985). anomuranhomologueofthiscrayfishstretchreceptorhasbeen
However, hippids’ superb adaptationtolife inthe swash zone found.
ofexposed sandy beaches, where they are tireless swimmers The hippid telson-uropod stretch receptor (examined in
and champions forspeedamongburrowing species (Duganet detailinEmeritaanalogaandE. talpoida:Paul, 1972;Pauland
al., 2000), required two evolutionary novelties in addition to Bruner, 1999;WilsonandPaul, 1990, andanatomicallyidenti-
rearrangements and modifications of ancestral neural and calinHippapacifica andE. austroafricanus: Paul, pers. obs.)
muscular traits: a muscle and a stretch receptor. The uropod is in a comparable position to the TUSRs in the tailflipping
NeurobiologyoftheAnomura 7
anomuransandit,too,respondstouropodelevationand,inpar- divergentbehaviours.Muchofthismaterialhas beenrecently
ticular,theuropodremotionbroughtaboutbycontractionofthe reviewed(Paul, 1991;Pauletal.,2002),sohereIwillhighlight
return-strokemuscle,uniquetohippoidsandmuchenlargedin afewoftheissuesandreferreaderstotheresearchpublications
Hippidae, asdescribedabove.However,thedifferentpositions forsubstantivedetailsandfurtherdiscussion.
of the somata and projections of the neurites of the sensory Neural networks driving repetitive movements such as
neurons in the sixth abdominal ganglion are strong evidence underly locomotion, respiration, chewing, and otherrhythmic
that the TUSRs in hippids and the tailflipping anomurans behaviours have atthen*core central patterngenerators (pace-
(Albuneidae, Galatheidae) are not homologues (Paul and maker neurons or small assemblies of neurons). The best
Wilson, 1994).Thehippidsensoryneuronsarealsophysiolog- known are thecentralpattern generators ofthe stomatogastric
icallydissimilar:theyarenonspiking,thatis,theyareincapable nervous system in crustaceans (Harris-Warrick et al., 1992).
of generating action potentials, as can the galatheids and The stomatogastric system is clearly an ancient network that
albuneidreceptors, butinsteadtransmit afferent signals inthe has been largely conserved morphologically. Variations in
form of graded depolarizations which mimic in form and physiological details (synaptic properties, neuromodulators,
amplitude the stretch applied to the receptor strand (Paul and etc.) havebeen uncovered, butnotextensively investigatedin
Bruner, 1999). Apparently the transformation of the stem thecontextofanomuranphytogenyorinrelationtotheecolo-
(albuneid-like?)hippoidtailfanintotheextraordinarytailfanof gy and habits of different species (Katz and Harris-Warrick,
hippids (Paul et al., 1985) included the replacement of the 1999).Pairedsegmentalpatterngeneratingmodulescontrolthe
ancestral, spikingtelson-uropod stretchreceptorby anew one limbsofcrustaceans, eachlimbbeing underthe controlofthe
thatostensibly servesthesamefunction,thatis, sensingeleva- adjacent hemiganglionic center (Mulloney and Hall, 2000
tionoftheuropodandactivatingresistancereflexesinhomol- Murchison et al., 1993). Much less is known about cellular
ogous uropod muscles. The caveat here, however, is that the composition and network operations of these hemigangionic
functional details, behaviouralroles, and synaptic connections centersthanaboutthestomatogastric system.Theyclearlydif-
are still poorly understood for any of these receptors. ferincellularcomposition-localintemeurons,manynonspik-
Nevertheless, itappearsthatduringhippidevolution,the spik- ing, form the core of the motor pattern-generating network,
ing sensoryneurons ofthereceptorintheirtailflipping ances- rather than motoneurons, as in the stomatogastric nervous
torswerenotconvertedtononspikingneurons,aswasinitially system, nevertheless largely similarmechanisms appearto be
assumed (Bush, 1976; Paul, 1991). Paul and Bruner (1999) used(e.g. gradedpotential,reciprocalinhibition,multiplicities
discussthehypothesisthatevolutionofthephysiologicalprop- of ion channels with differing kinetics). Testable hypotheses
erties of these nonspiking sensory neurons may have been about species dilferences can be formulated, therefore, even
determined by theirinterconnections withnonspiking cells in without complete knowledge of the particular pattern
thecentralpatterngeneratorforswimming. Observationsfrom generatorsinquestion.
two lines ofresearch in other reptantians suggest this hypo- Divergences in pereopoduse in posture and locomotionin
thesis. One is that certain swimmeret motoneurons are galatheids and hippoids, accompanying modifications in tho-
coupled to swimmeret interneurons in their hemiganglion racic segmentalmorphologyandendophragmal skeleton,have
(Heitler, 1978; Paul and Mulloney, 1985). The second is that been correlated with specific alterations in musculature,
nonspiking stretch receptors morphologically similar to those motoneurons, andmotorpatternsinvarious studies (Antonsen
inhippidsareinterconnectedwiththepatterngeneratorsforthe and Paul, 2000; Faulkes andPaul, 1997a, b, 1998). Each seg-
limb whose movement they monitor (thoracic walking legs: mental ganglion inthe ventral nerve cord ofcrustaceans con-
Sillar and Skorupski, 1986; abdominal swimmerets: Paul, tains a pair of central pattern generating circuits (one/limb)
1989b). Whatever the adaptive drive for the unusual physio- (Mulloney and Hall, 2000; Murchison et al., 1993).
logicalpropertiesofthehippids’ sensoryneurons,therepeated Interneuronal connections between hemiganglionic centers
appearance of telson-uropod stretch receptors in Anomura allowbilateral andlongitudinalcoordinationofmotoractivity
demonstrates that new types of neurons can be added to produced by these hemiganglionic centers (Namba and
inherited sensory-motor systems in the course ofbehavioural Mulloney, 1999).Theevolutionarypotentialofthisfunctional-
evolution. ly flexible aiTangement has been exploited extensively in the
evolution ofthe hippoid digging behaviour, a mosaic derived
Modularnei~voussystemsandcentralpattern generators. The by amalgamationoftwo disparate forms ofancestrallocomo-
evolutionary potential ofsegmental body plans has longbeen tion, walking and non-giant tailflipping (Faulkes and Paul,
recognized, and the ontogenetic mechanisms by which seg- 1997a, b, 1998). Laterdivergences ofphase couplings among
mental characters may be selectively lost, added, moved, or the digginglegs andbetweenthe legs and “tail” accompanied
modified are becoming apparent through the applications of divergence of the two sand crab families, Albuneidae and
geneticandmoleculartechniquestoavarietyoftaxaamenable Hippidae(FaulkesandPaul, 1997a,b, 1998;Fig. 1).
to such research (Giribet et al., 2001). Unfortunately, ano- Comparative neurobiological studies of other anomuran
murans,indeedmostcrustaceans,arenotamongthelatter,pri- behavioursarelikelytoprovideinferencesabouthowmodular
marily due to their complex life cycles. But fortunately, their systemsofneuronsfunctionandevolve,aswellasilluminating
segmental nervous systems are amenable to detailed mor- thebiology oftheAnomuraperse. Forexample, themodified
phological and physiological analyses, which allow detailed posture and gait of hermit crabs, associated with their
comparative investigation of the neural substrates for their asymmetrical abdomen and transport ofgastropod shells into
8 DorothyHaymanPaul
whichthey“retreat”rapidly(Chappie, 1966, 1973;Herreidand demonstrating that conserved and modified components of
Full, 1986), must have entailed changes in pereopod neuro- neuro-modulatory networks can be identified (Antonsen and
musculature and its central control. These remain to be Paul,2001,2002).Muchmoreresearchisneededtoclarifythe
explored. Snow’s (1975a, b) study of antennular flicking in functional organization of these aminergic systems and their
pagurids could also be profitably pursued. One may suppose interconnections with the rest of the nervous system in
thatflickingisunderlainbyhemiganglionicpattern-generating M. quadrispina, and other anomurans should be similarly
circuitry similar (serially homologous) to that controlling investigated. The variants in social behaviour evident among
pleopodsandpereopods(Murchisonetah, 1993). anomuran species constitute a largely untapped source of
The basal musculature of crustacean limbs is often information about mechanisms of neuromodulation and their
extremely complex and may include muscles with multiple evolution.
heads and specialized functions. Divergence in segmentally
repeated neuromuscular elements between segments in one Discussion
species and in the same segment in different species clearly
contributes to the postural and locomotory peculiarities of By placing the neural characters discussed above on a partial
individual species.Thisisillustratedbythe studyofAntonsen phylogenyoftheReptantiawhichincludesanomurans’closest
andPaul(2000)onthelegdepressormuscleinM.quadrispina, relatives (Fig. 1), several suppositions about neurobehavioral
which highlights the need for more, detailed analyses of the evolution in Anomura can be drawn. This exercise also both
functional morphology and innervation of such muscles, highlights under-studied groups and suggests experimentally
including the central structure of their motoneurons, in testable hypotheses aboutspecific neuronal systems in partic-
order to understand how the central neural networks (and ular species. The seven characters listed at the base, with the
neuromodulators, see below) produce species characteristic possibleexceptionofnonG(thecircuitryforrepetitivetailflip-
behaviours. pingthatdoesnotinvolveeithersetsofgiantinterneurons),are
ubiquitousamongmacrurandecapodgroups,includingnatant-
Neuromodulationandsocialbehaviours. Hormonesandneuro- iantaxa(Paul, 1989a;Pauletal., 1985),althoughtheyaremost
modulators regulate the expression ofthe moment-to-moment fully described in astacidean species, primarily of crayfish
behavioursproducedby sensory-motorsystemsemphasizedin (Wine, 1984).Thesecharactersarenotequivalentinthatsome
this review. They confer functional, as well as evolutionary, are individual neurons, whereas others are neuronal systems
flexibility on neurobehavioural networks (Katz and Harris- identified by their mediation of specific behaviours; few
Warrick, 1999).Theinvolvementofserotoninandoctopamine re-identifiableneuronsinthelatterhavebeendescribed,butas
inagonisticbehavioursofcrayfishandothercrustaceansiswell they becomeknown, they will constitute additional characters
known (Huberet al., 1997), but an understanding ofthe sites that willbeusefulforanalysisofneuro-behaviouralevolution
and mechanisms of action of these biogenic amines is very or in phylogenetic reconstructions. The losses preceding
incomplete (Panksepp and Huber, 2002). Unlike crayfish, and accompanying the divergence of the anomuran groups
Munida quadrispina (Galatheidae) neither form social hierar- included major elements ofmacrurans’ startle/escape systems
chiesnorfight,althoughduringagonisticencounters,theyper- (oneorbothofthegiantinterneurons-seeFig. 1 footnote 1),
formratherstereotypedgestures andbehavioursthatresemble aswellascertaincomponentsofthemassivetailneuromuscu-
those performed by dominant and subordinate crayfish lature,andwereseminalfortheanomuranradiation(Pauletal.,
(AntonsenandPaul, 1997).Nevertheless, asincrayfish,injec- 1985). Inparticular, the demiseofbothLGandMGinterneu-
tion of controlled doses of serotonin or octopamine into the rons in GalatheoideaandHippoidea wouldhavereducedcon-
hemolymph of M. quadrispina induces, respectively, “domi- straintsagainstmodificationoftailfanform,neuromusculature,
nant”or“subordinate”gesturesandbehavioursinisolatedani- and central motor systems controlling locomotion that were
mals (are they displaying to a phantom conspecific?). Most present in their macruran ancestors (Paul et al. 1985, 2002).
remarkably, serotonin-injected animals engage in full-blown Thispermittedthediversificationofmorphologyandbehaviour
fightswhenpairedwithanun-injectedindividual(whichtries, soevidentingalatheoidandhippoidanomurans.
unsuccessfully unless rescued by the experimenter, to retreat) The number of evolutionary modifications of retained
(AntonsenandPaul, 1997).EvidentlyM. quadrispinahavenot neural characters (hatched boxes in Fig. 1) is clearly a gross
lost the “fight center”, but the “interest in fighting”, perhaps underestimation, because, as explained above, most are func-
duetothelossofaparticularsynapse orexpressionofasero- tionalneuralnetworks (e.g.,thenonGcircuitryforswimming,
tonin (orother) receptor at some critical pointin the circuitry theCPGs,centralpatterngenerators, producingrhythmiclimb
involved in controlling agonistic behaviour (Antonsen and movements) in which an unknown number of neuronal and
Paul, 1997). Information on the social behaviours of other synapticchanges arelikelytohaveoccurred,butremaintobe
galatheidgeneraislargelylacking, andcircumspection should identified. One additional change in tailfan neuromusculature
be usedininterpreting differences inchelipedlength, orother not yet mentioned or included in Fig, 1 was pivotal to the
morphological characters, as indicators ofa species’ agonistic evolutionofthehippidsandcrabs’novelmodeofswimmingby
behaviour (Creasey et al., 2000). Comparisons of immuno- beating the uropods. This was the conversion of an axial
cytochemical maps of serotonergic and octopaminergic muscleintoanappendagemusclebychangingitsinsertion; in
neurons reveal both striking similarities and discrete differ- alltailflippingspecies(includinggalatheidsandalbuneids),the
ences between these systems inM. quadrispina and crayfish. PTF(posteriortelsonflexor)muscleistheterminalmemberof
NeurobiologyoftheAnomura 9
theconcatenated series offastflexormusclesthatmediatethe Other neural characters besides those included in Fig. 1
abdominal flexions or power strokes in tailflips (Dumont and confer evolutionary flexibility on neurobehavioural networks.
Wine, 1987).ThePTFhomologueinhippid sandcrabsinserts Inparticular, the complexity and subtlety ofneuromodulatory
ontheventralrimoftheuropodcoxa,adjacenttotheinsertion actionsatmanycentralandperipherallevelsisonlybeginning
oftheuropodpower-stroke muscle (homologueofthemacru- to be understood (Katz and Harris-Warrick, 1999; Panksepp
ran posterior telson-uropodalis muscle), so that, rather than andHuber,2002).Thepotentialforchangeatdiscretelociina
flexingthetelsononthe abdomen, itassistsinuropodpromo- neuromodulatory system to dramatically alter a species
tion during uropodbeating (Paul et ak, 1985). The homology behavioris exemplifiedby the loss inM. quadrispina of“the
between components of the power-stroke neuromusculature will”butnot“themeans” tofightconspecifics (Antonsenand
(musclesandmotoneurons)foruropodbeatingandtailflipping Paul(1997).Thediversebehaviours,generallysmallernumber
provides substantive evidence for the homology ofthe neural of neurons, and, in some cases, simplifications of circuitry
circuitries for swimming by uropod beating and tailflipping clearly make anomurans valuable subjects for many kinds of
(Fig. 1: nonG-»uropod beating). This hypothesis originated neurobiological research. Comparative investigations of their
withtheobservationthatathighfrequenciesofuropodbeating, nervous systems arebeginning torevealthe multiplelevels at
a small extension of the anterior abdomen occurs with each whichneuralevolutionoccurs.
uropod return stroke (= extension phase oftailflipping; Paul,
1971).Furthersupportforthehypothesisofhomologyofthese Acknowledgements
dissimilarbehavioursisthatrhythmicburstingofthemotoneu-
ronsinnervatingthePTFhomologueinhippidsisverypromi- Thanks to Adrian Wenner, University of California Santa
nentin the uropod motorpattern generated by isolated nerve Barbara,forthespecimensofHippapacificaandEmeritaaus-
cords ofEmerita analoga (Paul, 1979); i.e., uropod beating, troafricanus. The author’s research is supported by grant
likenonGtailflipping (Reichertetal. 1981), is organizedby a #8183-00fromtheNatural Science andEngineeringResearch
CouncilofCanada.
centralpattern-generatingcircuitthatdoes notrequire sensory
feedback to sustain its generation of alternating activity in
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