Mandibulate convergence in an armoured Cambrian stem chelicerate

20 Pages·2017·4.11 MB·English

by  Cédric Aria

AriaandCaronBMCEvolutionaryBiology (2017) 17:261
DOI10.1186/s12862-017-1088-7
RESEARCH ARTICLE Open Access
Mandibulate convergence in an armoured
Cambrian stem chelicerate
Cédric Aria1,4* and Jean-Bernard Caron1,2,3
Abstract
Background: Chelicerata represents a vast clade of mostlypredatory arthropods united by a distinctive body plan
throughout thePhanerozoic. Their origins,however, with respect to both theirancestral morphological features and
their related ecologies,are still poorly understood. In particular, it remains unclear whether their major diagnostic
characters were acquired early on, and their anatomical organization rapidly constrained, or if they emerged from a
stemlineage encompassing an array of structural variations, based ona more labile “panchelicerate”body plan.
Results: Inthisstudy,wereinvestigatedtheproblematicmiddleCambrianarthropodHabeliaoptataWalcottfromthe
BurgessShale,andfoundthatitwasacloserelativeofSanctacarisuncataBriggsandCollins(inHabeliida,ord.nov.),
bothretrievedinourBayesianphylogenyasstemchelicerates.Habeliapossessesanexoskeletoncoveredinnumerous
spinesandabipartitetelsonaslongastherestofthebody.Segmentsarearrangedintothreetagmata.Theprosoma
includesareducedappendagepossiblyprecursortothechelicera,raptorialendopodsconnectedtofivepairsof
outstandinglylargeandoverlappinggnathobasicbasipods,antennule-likeexopodsseeminglydissociatedfromthe
mainlimbaxis,and,posteriorly,apairofappendagesmorphologicallysimilartothoracicones.Whilethehead
configurationofhabeliidansanchorsaseven-segmentedprosomaasthechelicerategroundpattern,thepeculiarsize
andarrangementofgnathobasesandthepresenceofsensory/tactileappendagesalsopointtoanearlyconvergence
withthemasticatoryheadofmandibulates.
Conclusions:Althoughhabeliidansillustratetheearlyappearanceofsomediagnosticcheliceratefeaturesinthe
evolutionofeuarthropods,theuniqueconvergenceoftheircephalonswithmandibulateanatomiessuggeststhat
thesetraitsretainedanunusualvariabilityinthesetaxa.Thecommoninvolvementofstronggnathalappendages
acrossnon-megacheiranCambriantaxaalsoillustratesthatthespecializationoftheheadasthededicatedfood-
processingtagmawascriticaltotheemergenceofbothlineagesofextanteuarthropods—Chelicerataand
Mandibulata—andimpliesthatthisdiversificationwasfacilitatedbytheexpansionofdurophagousniches.
Keywords:Arthropoda,Chelicerata,Convergence,Macroevolution,Cambrian,BurgessShale
Background of “weird wonders” on a phylogenetic tree [3, 5, 10, 11],
Theearlyevolutionofarthropodshaslongbeenemblem- while the emphasis on divergences promotes the idea of
atic of the “Cambrian Explosion” [1, 2], and has grown unusualmorphologicalvariabilityintheearlyevolutionof
through the past decades into a remarkable variety of clades [2]. Homoplasies, by contrast, have received less
“stem” taxa [3–9], attracting emphasis on phylogenetic attentioninthatcontext[12].
similarities (homologies) and exceptional divergences In spite of being discarded when reconstructing phylo-
between morphologies. This is because morphological genetic relationships, phenotypic convergence remains
similarities of a common descent allow for the placement an informative (palaeo)biological observation, as it can
also illustrate the formidable morphological variability
*Correspondence:[email protected] deployed within or across body plans in response to
1DepartmentofEcologyandEvolutionaryBiology,UniversityofToronto, similar selective pressures [13–16]. In the Cambrian,
Toronto,ONM5S3B2,Canada
4Presentaddress:StateKeyLaboratoryofPalaeobiologyandStratigraphy, remarkable cases of convergence have been documented
NanjingInstituteofGeologyandPalaeontology,ChineseAcademyof in which body plans or appendages are reminiscent of
Sciences,Nanjing210008,China
derived taxa due to the early occupation of the same
Fulllistofauthorinformationisavailableattheendofthearticle
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InternationalLicense(http://creativecommons.org/licenses/by/4.0/),whichpermitsunrestricteduse,distribution,and
reproductioninanymedium,providedyougiveappropriatecredittotheoriginalauthor(s)andthesource,providealinkto
theCreativeCommonslicense,andindicateifchangesweremade.TheCreativeCommonsPublicDomainDedicationwaiver
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AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page2of20
niches [17, 18]. At the same time, convergences are well Sanctacaris [26], as originally proposed by Briggs and
known to outline some of the structural constraints Collins [32]. Sanctacaris has been shown so far to dis-
shared by different groups of species. A prominent case play a five- or six-segmented cephalon, a condition
of convergence involving all types of Palaeozoic and closer to the euchelicerate condition (six-segmented)
extant euarthropods is the distal differentiation of than the four-segmented head of megacheirans. Howe-
appendagesinto pincers[9,12]. ver—and there lies the conundrum—, in addition to sev-
Broad morpho-functional convergences may be less eral uncertainties regarding its head configuration, such
expected between early-diverging lineages, as we would as the forward attachment of its raptorial limbs in a
think that recently selected traits would provide greater “bundle,” Sanctacaris lacksaclear indicationofachelate
fitness for the exploration of new niches, and that frontalmost appendage comparable to the chelicera. A
disruptive selection would impact the phenotype at lar- series of very recent studies have documented other
ge—even when considering the role of mosaic evolution. forms with likely affinities to Sanctacaris from the
Thus, for instance, early representatives of the two ex- Spence and Wheeler Shales in Utah [33, 34] and the
tant euarthropod clades, Chelicerata and Mandibulata, Emu Bay Shale in Australia [35], but this particular un-
would have been morphologically diverging rather than certaintystillremains.
converging, developing different morpho-functional ad- It may also be considered that both megacheirans (or
aptations and “maturing” their respective body plans to atleast someofthem)andSanctacaris-likemorphotypes
form the basis of their great diversification during the are partof the chelicerate lineage, with Sanctacarisbear-
Phanerozoic. ing, for instance, very reduced great appendages. This
However, little is still known about the origin per se of idea would conflict with a scenario in which antennule-
extant lineages and about the significance of Cambrian bearing artiopodans (and in particular xenopodans, i.e.,
high evolutionary rates [19] and, questionably [20, 21], Sidneyia and Emeraldella) would constitute the basal-
exceptional morphological variability [2, 22, 23] on their most part of this lineage, based mainly on a comparison
stem taxa. We recently proposed a scenario for the early between their exopod morphology and the gill opercula
radiation of Mandibulata based on a reevaluation of of euchelicerates [26]. Such comparison remains tenta-
bivalved arthropod anatomy [9], which represents a new tive, however, and further assessment of possible cheli-
avenue of research based on adult macrofossils to ex- cerate affinities are notably hampered by a limited
plore these questions. The origin of chelicerates, on the knowledgeofthexenopodanhead anatomy.
other hand, has been the subject of some more active In this study, we thoroughly reinvestigated the Burgess
debate in recent years [24–28]. Based on the topology Shale euarthropod Habelia Walcott, 1912 based on
and structural similarity between chelicerae and “great Walcott’s original material and new specimens discov-
appendages,” some authors [24, 25, 29] have proposed a ered by the Royal Ontario Museum. Habelia optata was
phylogenetic continuity between these frontal limbs. Al- initially regarded by Walcott as an “aglaspidid meros-
thoughthisdoesnotimplythatmegacheirans(bearingthe tome,” which would hint at a chelicerate affinity [36],
great appendages) and chelicerates necessarily form a but this statement lacked much justification [37]. Simo-
clade, this has been hypothesized as such [12, 28, 30, 31], netta [38] and Simonetta and Delle Cave [39] followed
assumingthatthechelatenatureoftheseappendagescon- this view based mostly on overall aspect, while prefer-
stitutesanapomorphyforthesetaxa,contrastingwiththe ring to compare H. brevicauda, the new morphotype
antennular anteriormost appendages present in other erected by Simonetta, to Leanchoilia [39]—a mega-
euarthropods. cheiran. Importantly, early authors [37–41] recognized
Although the grouping of megacheirans with chelice- the presence of at least five pairs of head appendages,
rates has been retrieved phylogenetically [6], it has been a condition that could have later related this animal
shown to be a possible methodological (polarization) to Sanctacaris—even if an interpretation of strictly
bias associated with the retrieval of Arachnomorpha five pairs and some other morphological details led to
under parsimony [27]. More recent analyses have found comparisons with crustaceans instead [40, 42]. In his
megacheirans (or, at least, cheiromorphs) to be more revision of the genus, however, Whittington [43]
basal, possibly forming a sister group to artiopodans and rejected previous interpretations of a cephalon with
extant clades [8, 9]. Apart from considering great ap- five head appendages or more, leaving Habelia as a
pendages to be the direct precursors of the chelicerae, problematicum.
there does not seem indeed to be any unambiguous Herafter, we reevaluate the significance of Habelia
character supporting the placement of megacheirans on for the early evolution of chelicerates, as well as for
the cheliceratelineage. the understanding of morphological convergence in
Instead of megacheirans, the groundplan of chelice- the ecological context of the radiation of Cambrian
rates could be represented by the Burgess Shale species euarthropods.
AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page3of20
Methods Abbreviationsandterminology
Fossilmaterialandobservation Abbreviations used in figures: ag, anterior gnathobase;
Most specimens were collected in situ from the Greater am, arthrodial membrane; an, anus; ap, anal pouch; att,
Phyllopod Bed within the Burgess Shale Walcott Quarry, endopod attachment on gnathobase; bas, basipod(s); ce,
inYohoNationalPark,BritishColumbia.Twoadditional cephalic endopod(s); cen, cephalic endopod n; cel, left
specimens come from other Burgess Shale localities (see cephalic exopods; cpl, cephalic pleura; cx, cephalic exo-
Additional file 1 for a detailed list of studied specimens). pod(s); cxn, cephalic exopod n; db, distal brush; dpex,
41 specimens were studied in total, including 14 from distal part of exopod; ds, dorsal spine; dtp; distal telson
the National Museum of Natural History, Washington piece; e, eye; en, endopod n; en, endopod; ex, exopod;
D.C. (USNM), and 27 new specimens from the Royal das, dark stain; g, gnathobase(s); gnl, left gnathobase n;
Ontario Museum Invertebrate Palaeontology collections gnr, right gnathobase n; hyp, hypostome; ia, intermedi-
in Toronto (ROMIP). Methodology for observation ary appendage; it, intestine; jt, joint; la, labrum; m,
followed our previous studies on Burgess Shale arthro- mouth; nv?, nerve?; oe, oesophagus; pn, podomere n;
pods [9, 27, 44]. Selected specimens were mechanically pex, posterior exopod(s); pexn, posterior exopod n;
prepared to remove matrix covering anatomical features. ppex, proximal part of exopod; ptp, proximal telson
All material was observed under a stereomicroscope piece; rap, reduced anterior appendage(s); st, stomach;
equipped with polarizing filters, and photographed both tn, thoracic appendage n; te, thoracic endopod(s); tel.,
dry and wet under natural and cross-polarized lighting, telson, ten, thoracic endopod n; th, telson head; tpl,
occasionally using ammonium chloride sublimate to trunk pleura(e). Hereafter, we call “gnathobasic append-
highlightthree-dimensionaldetails. age” an appendage whose basipod is gnathobasic, that
is, differentiated into a masticatory structure (more
Phylogeneticanalyses strongly sclerotized, often bearing ornaments such as
We used a Bayesian technique oftree search on a revised setae and teeth).
version of a previously published dataset [9], now com-
prising77taxaand215characters,allunweightedandun- Results
ordered(seeAdditionalfile2,ref.[9]foroverallcharacter Systematicpalaeontology
descriptions and Additional file 1 for improvements), and Superphylum Panarthropoda Nielsen,1995.
with inapplicable entries treated as uncertainties. The PhylumEuarthropoda Lankester,1904.
topology was generated using MrBayes v.3.2.6 [45], with Clade Arachnomorpha Heider, 1913 (= Arachnata
parametersettingsfollowingtheMkvmethod[46].Asper Lauterbach,1973).
MrBayes’ restrictions, Priapulida was used as the single Diagnosis (emended from Størmer, 1944). Euarthro-
outgroup (following refs. [47, 48]), but was subsequently pods with the following characters: Cephalic shield
retrieved in a polytomy with Nematoda. Trees were pro- encompassing at least four pairs of appendages with
ducedduringfourrunsof5,000,000generationswithfour well-developed endopods; originally, presence along
parallel chains, a tree sampled every 1000 generation and body of at least one pair of appendages with basipod
burn-inof20%.Among-characterratesweresettoremain differentiated into a well-sclerotized gnathal sclerite
equal.ABayesiantreatmentofourdatawaschosentoex- bearing setae or teeth (“gnathobasic appendage”); third
plore an alternative methodology to parsimony, which is gnathobasic cephalic appendage also part of groundplan;
particularly sensitive to the suboptimal treatment of in- post-cephalic endopods terminating in a trident of claws
applicable states [27]. Bayesian analyses have also been withvariousarrangements.
shown to provide more accurate results than parsimony, Order Habeliida,ord.nov.Aria andCaron
albeitwithapossiblelossofprecision[49,50].Inorderto Type family. Habeliidae Simonetta and Delle Cave,
account for the morphological and molecular signal that 1975.
canonlybecodedamongextanttaxa,wechosetoapplya Other included taxa. Sanctacarididae Legg and Pates,
backboneconstraintonourdataset,basedonthetopology 2016.
of Regier et al. [51]. As in ref. [9], we preferred this Diagnosis.Arachnomorpharthropodswiththefollow-
method over the direct implementation of numerous ing characters: Cephalic shield with sub-triangular, sub-
extant-only characters to avoid overburdening the horizontal pleural expansions and with antero-lateral
dataset with question marks, which causes instability notches accommodating pair of lateral compound eyes
and a lack of resolution in (relatively) small datasets with no peduncle; cephalic shield with large mesio-
[52, 53]. Finding inconsistencies of placement with dorsal bulge accommodating stomach; five pairs of an-
different codings of the head anatomy, pycnogonids terior, slender and segmented antennule-like exopods
were removed from the analysis presented here (see likely inserted below the eyes and dorsally to other head
Phylogenetic results). appendages; on ventral side of head, reduced pair of
AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page4of20
appendages inserted anteriormost (presumed in Sancta- of cephalon and posterior portion of trunk segments
carididae), followed by five pairs of appendages richly adorned with small blunt spines/tubercles; ceph-
composed of gnathobasic basipods increasing in size alic gnathobases with elongate proximal “arm”; gnatho-
posteriad and bearing seven-segmented spinose/setose basic teeth differentiated antero-posteriorly (slender and
enditic endopods projecting anteriad; trunk bearing long to short and stout); cephalic endopods with setal
paddle-like exopods fringedwith thinlamellae. brush on podomeres 5 and 6; five-segmented thorax
Remarks. We maintain the family Sanctacarididae bearing strong biramous appendages with robust, clawed
erected by Legg and Pates [33], since 10 trunk segments endopods and long basipods; very long (subequal to
and a spatulate telson remain diagnostic of Sanctacaris slightly greater than head and trunk length) bipartite tel-
uncata, Utahcaris orion [33] and Wisangocaris barbara- son, with a long, dentate proximal portion adorned with
hardyae [35]. The affinity of Messorocaris magna [34] is lateral spines, and a short distal portion about 1/3rd as
less clear, but the peculiar shape of its trunk pleurae long asproximalportion.
mayplace itinitsownfamily. Description. Habitus. Body 8.5 to 34 mm (without
Habelia had previously been assigned to the orders telson), elongate, 19-segmented and tagmatized (Fig. 1):
Aglaspina by Walcott and Emeraldellia by Størmer [36]. cephalon (seven segments with tergites fused in a single
Given the lack of cladistic support for these taxa, shield) (Figs. 1, 2a–g), trunk (12 segments) (Fig. 1),
which would be para- or polyphyletically nested within tailpiece (bipartite) (Fig. 1); trunk subdivided into tagma
Arachnomorpha,thelackofredescriptionforMolaria,and II/“mesosoma” (five anteriormost segments) and tagma
thefactthattheirdiagnosesshouldbeextensivelyrevisedin III/“metasoma” (Fig. 1); “mesosoma” bearing robust
light of the new data gathered on aglaspidids and Emeral- walking legs (Fig. 1); tailpiece a very long (ca. length of
della,wehavenotreusedAglaspinaorEmeraldelliaherein. cephalon and trunk) and slender spiniform telson with
FamilyHabeliidae Simonetta andDelleCave,1975. articulatedterminalpiece(Fig. 1f,g).
Type genus. HabeliaWalcott,1912. Cephalon (“prosoma”). About 30% of trunk length;
Diagnosis. Habeliidan euarthropods with the following length about 80% of width (Fig. 1). Composed of a cen-
characters:Bodyelongate,19-segmented,dividedintothree tral, bulging area, housing the stomach, and of lateral
distinct tagmata: cephalon (or “prosoma”) of seven seg- pleural expansions of the tergal shield, sub-aligned with
ments (or eight somites) and trunk (12 segments) com- the frontal plane (Fig. 2g and Additional file 3,
posed of a five-segmented thorax (or “mesosoma”) and Additional file 4, Additional file 5, Additional file 6,
eight-segmented post-thorax (or “metasoma”); trunk tag- Additional file 7). Broad and sub-triangular in dorsal
matization based on discrete limb differentiation between view, with antero-medial margin separated from lateral
thorax and post-thorax; posteriormost cephalic appendage (pleural) margins by strong ocular notches (Figs. 1b, 2a
(7th) similar to thoracic appendages, all characterized by a and Additional file 3, Additional file 4, Additional file 5).
cheiromorph morphology: large undifferentiated basipods, In lateral view, dorsal section of the cephalic shield high
well-developedseven-segmentedendopodswithoutendites, and sub-convex with relatively longer anterior face; ocu-
andpaddle-likeexopodsfringedwithoblanceolatelamellae; lar notch strongly impressed at the anterior junction be-
telsonelongate. tween dorsal and postero-lateral sections of head shield;
Remarks.Wehereby establishadiagnosisforthefam- cephalic pleurae usually not visible in lateral view, due
ily Habeliidae, as the original publication of the taxon to their sub-horizontal position (Figs. 1, 2a, b). Pleural
was not associated with one [39]; we also formalize margins of the cephalic shield adorned with short, tri-
diagnoses and descriptions for Habelia optata hereafter. angular spines (Fig. 2g and Additional file 6, Additional
The genus Thelxiope was also included in Habeliidae by file 7); cephalic shield adorned on its entire surface with
Simonetta and Delle Cave; however, the presence of numerous,scatteredshortandblunt spines(Fig. 1b, h).
eight post-cephalic tergites and a pygidium would rather Eyes. Presence of a pair of spherical lateral eyes,
seem to indicate a relationship with Mollisonia [54, 55]. presumably compound, inserted at the anterior
Thelxiopeistherefore removedfrom Habeliidae. notches between dorso-medial head bulge and lateral
Genus Habelia Walcott,1912. pleurae; approximately the size of the notches, i.e.
(Figures 1, 2, 3, 4; Additional file 3, Additional file 4, 14% of head length in diameter; no trace of peduncle
Additional file 5, Additional file 6, Additional file 7 and (Figs. 1a–d, 2a, g).
Additionalfile8) Hypostome-labrum complex. The anteriormost margin
Type species.HabeliaoptataWalcott,1912. of the body bears medially a structural complex com-
Diagnosis. Habeliid arthropod with the following posed of dorsal and ventral elements, homologized here
characters: Post-ocular lateral and postero-lateral ceph- with labrumandhypostome.
alic margins as well as pleural margins of trunk seg- Labrum. Anteriormost is a bulging body protrusion
ments adorned with triangular spines; cuticular surface with length ca. 13% of head length, with rounded
AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page5of20
Fig.1GeneralanatomyofHabeliaoptata,morphsA(d-g)andB(a-c,h).aROMIP64357.bUSNM139209(insetis(h)).cROMIP64358.dROMIP
64359.eClose-upofthemandiblesonthecounterpartof(d)(wetspecimen).fClose-upofthedistaltelsonpiecein(g)(wetspecimen).gHolotype
USNM57693(insetis(f)).hClose-uponcephalicornamentationakintotrilobiteprosoponin(b).Allpicturestakenundercross-polarizedlight.For
abbreviations,seeMethods.Scalebars:(a),4mm;(b),3mm;(c,d,g),2mm;(e,f,h),1mm
anterior margin slightly extending beyond head shield in a series of branched antennule-like appendages and a
dorsalview, andinterpretedasalabrum(Fig. 2g,i). series of five large, elongate, toothed, forward-oriented
Hypostome. In ventral view, a sclerite with possible gnathobases bearing seven-segmented elongate spinose
midline separation beneath the frontal protrusion (la- legs (Figs. 1, 2); an additional pair of appendages, with
brum) isinterpretedasahypostome(Fig. 2g). broad, rounded exopods and well-developed endopods,
Mouth. Mouth opening located very anteriorly, is located between the cephalon and trunk, but likely
above first pair of gnathobases, and opening ventrally belongs to the cephalic tagma in the absence of dedi-
(Figs. 1c, 2d). cated trunk tergite (Figs. 1b, 2a, g and Additional file 5,
Alimentary tract. Gut differentiated into foregut, Additionalfile6).
stomach and intestine; foregut directed dorsally (“oe” in Frontal-most appendage pair. Flexible (articulated?)
Fig. 2d), gently curving posteriorly towards a large stom- and very short (about half the length of the following
ach; stomach much wider than deep, occupying most of first gnathobasic appendage’s endopod) (Fig. 2i–m); ter-
head space and partly housed within a dorsal bulge of minationunclear,clawpossiblypresent (Fig. 2i).
the cephalon (Fig. 1d); stomach constricted at the pos- Post-frontal series of appendages. Five pairs of hyper-
terior margin of cephalon to form the intestine, ca. 1/4 trophied gnathobases occupy most of ventral space
of body width, tapering to trunk segment 5, and finally under head shield (Figs. 1, 2); gnathobases with toothed,
reduced to a much smaller (ca. 1/3 of anterior diameter) straight masticatory margin parallel to ventral margin
duct in trunk segment 6 (Fig. 1c–g); anus opening pos- concentrated ca. within the anterior first 40% of head
teriorlyin anal pouch (Fig. 1a-d, g;see “tailpiece” section length (in short succession), so that the portion between
below). masticatory margin and attachment (“arm”) is increas-
Cephalic appendages. Post-ocular appendicular head ingly elongated inposteriorgnathobases—reachingupto
composed of a pair of reduced frontal-most appendages, ca. 50% of head shield length for appendage 5 (Figs. 1c,
AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page6of20
Fig.2AnatomicalandmorphologicaldetailsofHabeliaoptata,morphsA(b,d,f,n)andB(a,e,g,i,l,m).aUSNM139209,close-upofanteriorcephalic
area,showingintermediaryappendage.bUSNM268931,cephalon,showingsuperimposedinsertionofendopodsongnathobases;starpointsto
insertionofanteriorendopods.cROMIP64357,close-upoffourthcephalicexopodialbranch,distalportionshowingslenderpodomeres;arrowpointsto
tridentofsetaeatpodomerejunction.dROMIP64358,close-upofanteriormostregion,showingmouthopeningandfirstanteriorpairsofgnathobases.
eROMIP64360,close-upofteethonmasticatorymarginofgnathobase;noteheavyconcentrationofcarboninteeth.fClose-upofteethonmasticatory
marginofposteriorgnathobaseonsamespecimenasinD,showingstrongercarboncontentindentaledge.gROMIP64364,specimenpreservedin
ventralaspect,close-upofanteriorregionshowinglabrum,eyesandappendages;starmarksattachmentoffifthspinoseendopod;arrowpointsat
ornamentalspineofcephalicpleura;insetsasindicated.hROMIP64362,close-upofposteriortrunkexopods.iROMIP64363,close-upofanteriorright
cephalicregion,dorsalviewshowinglabrumandappendages;arrowspointtooverprintofgnathobasesunderneathcephalon.j,kROMIP64364.
jClose-upofdistalportionofcephalicendopod,showing“platform”withsetalbrushes.kClose-upofterminalclaw;arrowspointtoteethoninner
marginofclaw.lUSNM144907,close-upofcephalicgnathobases;arrowspointtodentatemarginsofopposinggnathobases.mROMIP64357,close-up
onanteriorleftcephalicregion,showingappendages;arrowpointstoanteriorinsertionoffourthcephalicendopod.nROMIP64359,close-upofcephalic
appendagesshowinginsertionofendopodsongnathobases;starmarksattachmentoffourthcephalicendopodonitsgnathobase.c-f,jandkare
SEMimages;allotherarestereomicroscopeimagesofdryspecimensundercross-polarizedlighting.Forabbreviations,seeMethods.Scalebars:
(a,g,h,i,l,n),1mm;(b,m),0.5mm;(c,d,k),200μm;(e),100μm;(f),50μm;(j),500μm
g, 2b, d); overall size of gnathobase also increasing pos- proximal margins; distalmost portion of masticatory
teriad, with anteriormost gnathobase inclusive of teeth margin pointing outward (Fig. 1e); from gnathobasic ap-
roughly as wide as half the labrum (2B, D, G, L, N) and pendage 3 to 1, teeth increasingly more slender, sharper
posteriormost gnathobase with length of masticatory and longer in relative size, so that the anteriormost
margin around a 1/4th of head length (Fig. 1c-e, g); gnathobase displays a morphology (short armature with
gnathobases extensively overlapping (Figs. 1c, g, 2b, l); long and slender teeth) substantially different from
masticatory margin with ca. 18 longer and shorter teeth posteriormost (long armature with shorter, blunt, more
arranged in two staggered rows, so that long and short robust teeth) (Fig. 2d,n).
teeth imbricate when opposing margins are closed; all Endopods seven-segmented, gradually increasing in
teethstronglysclerotized(Figs.1c-e,g,2d-f,n);bothsets sizeposteriorward,from40%of headlengthtotwicethis
of teeth gradually decreasing in size proximalward; mas- size, with a distinctly larger increase between legs 3 and
ticatory margin with convex latero-distal and latero- 4 (Figs. 1c, d, 2g–m); bent proximally and forming an
AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page7of20
Fig.3DiagrammaticreconstructionofHabeliaoptata,morphA.aVentralviewofthecephalon.Right“intermediary”appendageremovedto
showgnathobasemorphology.bLateralview.cDorsalview.dIsolatedbiramousthoraciclimbinfrontal,lateralandposteriorviews(leftto
right).Forabbreviations,seeMethods.LinedrawingscourtesyofJoannaLiang©RoyalOntarioMuseum
almost 90 degree angle between podomeres 2 and 4; Exopods are represented by five long and slender rami
podomere size formula is [x / x+(1/5)x / x+(2/5)x / x made of seven or more podomeres (Figs. 1, 2); each seg-
+(1/5)x / x+(2/5)x / x / x (claw)] proximo-distally; ter- mentaljunction bearsthree stiff setae (Fig.2c);distalmost
minal podomere a strong claw with two successive teeth unit bears at least three setae; podomeres with diameter
on its ventral margin and adjoined by a pair of smaller, distinctly reduced proximal-ward and sub-concave mar-
slender claws posteriorly (Fig. 2k); at least podomeres 2 gins (Fig. 2c); length of each subsequent podomere is ca.
and 3 bear well-developed enditic projections on their 20% greater than preceding podomere (Fig. 1a); all rami
distalmost margins, forming platforms where insert bun- increasing gradually in size posteriorward, but first ramus
dles of more than 9 setae, of which the three central distinctlyshorter,onlyslightlylongerthanendopodoffirst
ones are more robust (Fig. 2j); proximalmost podomere gnathobasic appendage (Fig. 2i); attachment unclear, but
(1) of each endopod inserts on distal margin of corre- does not appeartobeonmain branch ofgnathobasic ap-
sponding gnathobase, close to the distal border of the pendages;fifthramusapartfromtheothersindorsalview
masticatorymargin(Fig.2n). and projecting more laterally close to the endopod of the
Fig.4ArtisticreconstructionofHabeliaoptata.CourtesyofJoannaLiang©RoyalOntarioMuseum
AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page8of20
fifthgnathobasicappendage,suggestingadifferentattach- Endopod seven-segmented (six podomeres plus a
ment (Fig. 2g and Additional file 3, Additional file 5, claw); first (proximalmost) podomere quadrate, podo-
Additionalfile7). mere size formula [x / x / x+(1/3)x / x+(1/4)x / x+(1/3)x
7th head appendage. One pair of biramous append- / x+(1/2)x / (3/4)x (claw)] proximo-distally (Fig. 1a-c, g
ages located at junction between cephalon and trunk and Additional files 4, Additional file 5, Additional file 6,
(“ia” in Figs. 1a, b, 2a, g, 3a); morphology similar to Additional file 7); mesio-distal margins of podomeres
thoracic appendages, but reduced to ca. 2/3 of length forming thickened rims; terminal claw strong, length
of first three trunk pairs; exopod more circular with about half of podomere 6, adjoined posteriorly by two
finer and more numerous lamellae (Figs. 1b, 2a and smaller slender claws (Fig. 1a and Additional files 4,
Additional files). Additionalfile5,Additionalfile6,Additionalfile7).
Trunk (“opisthosoma”). Tergo-pleurae. 12-segmented, Exopods paddle-like, margins fringed with thin lamel-
anatomically divided into anterior (five first segments, lar setae except on the most proximal left and right
thorax or “mesosoma”) and posterior (post-thorax or thirds; paddle connected to an attachment podomere
“metasoma”) tagmata (Fig. 1); segments forming strongly inserted via an elongate hinge on the distal half of the
bipartite tergo-pleurae, with an anterior portion (“doub- basipod; exopod length about 2/3rd of endopod (Figs.
lure”) mostly unadorned on its surface and a stronger, 1b, 2aandAdditionalfile6).
elevated posterior portion (“armature”) covered in short Post-thoracic appendages. Broad, sub-spherical exopods
blunt spines (similar to the surface of head shield) and slightlyjuttingoutbeneathpleuraefrom segment 6to12;
produced into paired dorsal projections adorned with exopod size decreasing gradually to segment 11 (Fig. 2h);
longer and sharper spines (Fig. 1); upper antero-lateral exopod of last segment much smaller; no adornment vis-
margin of armature fused with doublure, so that the dis- ible;endopodspresumablyreducedorabsent.
continuity between doublure and armature is more pro- Tailpiece. Tailpieceaverylong(subequaltoslightlylon-
nounced on pleura and posterior side of segment ger than head and trunk combined), bipartite, telson with
(Additional files 3, 4); margin of doublure produced on spinose lateral margins (Fig. 1); first piece composed of a
its pleural circumference into sharp lanceolate spines broad “base” (telson head) on the first 1/9th of its length
growing more elongate distalward, with longest spines andofanelongate,muchthinnerposteriorrod-likeexten-
(ca. 2/3rd of segment length) on the posterior side of sion with gentle dorsal concave curvature (Fig. 1a–g); on
pleural distal extremity (Fig. 1b–g); margin of pleural dorsal side of base, parallelcarinae converging from posi-
part of armature adorned with minute spines; length of tions of trunk protrusions on trunk tergites and running
upper doublure less than half armature length in anter- entirelengthoffirsttelsonpiece(Fig.1a–g);ventralsideof
ior segments but increasing posteriad to reach about base protruding, with sharp anterior slope, sub-straight
identical length with armature; doublure width reducing margin pointing dorso-posteriorly and curved margin join-
on anterior side of pleura up to fusing with armature ing with more slender part of telson piece (Fig. 1a, b); an
margin; on posterior side of pleura, margin of doublure oblong cuticular structure, the anal pouch, is attached to
closely parallel to margin of armature (Fig. 1b–g); anter- sub-straight margin of some specimens, pointing postero-
ior pleurae sub-horizontal, from segment 3 posterior- ventrally(Fig.1);lengthofanalpouchabout12%oflength
ward gradually more parallel to body axis; pleura of first of first telson piece; lateral spines sharp, decreasing in size
segment about 3/4th of cephalic pleura length, pleura of posteriad, all successive except for first two spines on base
second segment subequal to cephalic pleura, pleura of closertooneanotherthantofollowingspine,itselffollowed
third segment slightly longer than cephalic pleura, by a gap before the next; second telson piece a straight ar-
posterior pleurae gradually decreasing in size, except for ticulating rod about 1/3rd of first telson piece length and
pleura of last segment, forming an elongate blunt blade endinginasetofthreesetae(Fig.1f).
reaching back of telson base (Fig. 1b–g); margins of Remarks. We found Habelia brevicauda [38] to be-
doublure and armature also increasingly curved long outside habeliidans, and the revision of this taxon
posteriad. istheobjectofacurrent study.
Thoracic appendages. Biramous with well-developed Habelia optataWalcott,1912.
endopods, present in trunk segments 1 to 5 (Fig. 1); Synonymy
appendages in segments 1–3 subequal, attachment to tip
of endopod about 120% of head length; endopods of 1912Walcott,pp.202–203,pl.29,fig.6
appendages 4 and 5 distinctly longer than 1–3, with 1920Raymond,pp.120–121
endopod 5 also slightly longer than 4 (Fig. 1 and 1920Henricksen,pp.16
Additionalfiles 5,Additionalfile6,Additionalfile7). 1944Størmer,p.86
Basipod broad and cylindrical, ca. 1/3rd of endopod 1959Størmer,inMoore, p.31,figs.19,3(copyof
length (Fig. 1bandAdditionalfile6). Walcott(1912))
AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page9of20
1964Simonetta,pp.219–222,fig.2,pl.xxxvi, The Chelicerata clade is composed of paraphyletic “mer-
unnumbered figures ofUSNM 57693,139,209, ostomes” (xiphosurans, eurypterids and chasmataspi-
144,907–909 dids), from which emerges a monophyletic Arachnida.
1975SimonettaandDelleCave, pp.27,32,pl. iii,fig2a, This topological arrangement is broadly consistent with
b(reproducedfromSimonetta (1964)),pl.xxi,figs.1-3, the latest fossil-inclusive studies investigating chelicerate
figures ofsamespecimens asSimonetta (1964) relationships [30, 56]. Contra [30], however, we find
1981Whittington, pp.343–346,fig.61;figs.62–66, Offacolus and Dibasterium to lie as sister taxa to all
plate 7;figs.67–71, plate8;figs.72,75–77; figs.78–83, other euchelicerates (as in [56, 57]), in contiguity with
plate 9,fig.130 habeliidans.
In the topology presented here, Chelicerata is equiva-
Diagnosis. As per genus. Morph A (Figs. 1d-g, 3, 4 lent to Euchelicerata because we removed Pycnogonida
and Additional files 4A–D, 7E, F, J, K): First three anter- from the analysis. Thephylogenetic position of pycnogo-
ior dorsal trunk projections long, with first longest nids has long been an issue [47, 51, 58], and morpho-
(about 45% of head length), second slightly shorter than logically the presence of uniramous endopods (derived
first and third slightly shorter than second; first projec- foreuchelicerates)witha(possibly)four-segmentedhead
tion pointing dorsally and other two pointing increas- tagma (plesiomorphic for arachnomorphs) are character
ingly posteriad; antero-proximal portion of projections states that are highly conflicting in this particular topo-
sub-straight, so that distal portions of projections 2 and logy—especially with the inclusion of Habelia. Because
3 form an obtuse angle with that base; first pair of of this, coding pycnogonids with a four-segmented head
projections with antero-proximal base forming convex places them with Marrella at the base of the Artiopoda,
margin in lateral view; posterior dorsal projections whereas a seven-segmented coding affects the position
convex dorsally, rounded anteriorly and pointed poster- of Offacolus and Dibasterium, bringing Limulus and
iorly. Morph B (Fig. 1a-c, h and Additional files 3, Weinbergina as basalmost (due to their loss of exopods).
Additional file 5, Additional file 6, 7A–D, G-I): Five We consider hereafter that pycnogonids still define
anterior-most pairs of dorsal spinose elevations forming Chelicerata as sister group to euchelicerates (i.e., branch-
rounded mounts decreasing in size posteriad and differ- ing immediately following habeliidans), but their exact
entiated so that the pointed posterior end is moderately phylogeneticplacementwillrequirefurtherinvestigation.
raised dorsalward: angle of posterior spinose projection In concordance with [56, 57], we retrieve Chasmatas-
with longitudinal plane of body ca. 70° in ts6, 80° in ts5 pis and Megalograptus as paraphyletic, but Limulus and
(but with more rounded aspect) and 85° in ts4–1; orna- Weinbergina as forming a clade. This could be due to
mental spines stronger, longer and more numerous on our limited taxon sampling. The retrieval of cheiro-
ts1–5; posterior dorsal projections convex dorsally, morphs as part of a merostome clade by Garwood and
roundedanteriorlyandpointedposteriorly. Dunlop [30] may illustrate a problem of character
Description.Asper genusanddiagnosis. polarization acrosshigher nodes.
Remarks. Morphs A and B are clearly discriminated A notable difference with the previous analysis of this
bythepresenceofanteriordorsalspines,with noindica- dataset under parsimony [9] is the retrieval of Arachno-
tion of intermediaries, and no obvious relationship to morpha sensu Störmer [36], that is, the monophyletic
overall size. This dichotomy does not overlap with the group composed of Trilobitomorpha sensu lato (or
presence of “anal pouch,” as the latter can be either Artiopoda sensu Hou and Bergström [4]) and Chelicer-
present or absent in specimens with dorsal spines. It is ata. It has been recently shown that Arachnomorpha
worth noting that specimens with and without elongate could result from a polarization bias overweighting the
trunk spines as well as specimens with or without anal absence of characters in a dataset, for instance when
pouch co-occur on the same stratigraphic levels within coding inapplicable entries as additional states [27]. The
the Walcott quarry (Additional file 1). This supports the fact that we retrieve here this clade using a Bayesian
idea, on the basis of niche distribution, that these traits approach instead of parsimony, and after coding in-
are conspecific, and that one of them likely character- applicable entries as uncertainties, suggests that the
izes sexual dimorphism. For this reason, we refrain grouping of trilobitomorphs with chelicerates exclud-
from erecting distinct morphospecies based on these ing cheiromorphs (contra Arachnomorpha retrieved in
morphs, and both are considered for now to belong to refs. [6, 27]) is a resilient configuration. Such resili-
H. optata. ence to methodological variations is further supported
by the fact that these taxa have also been found to be
Phylogeneticresults monophyletic using implied weighting [8].
Our Bayesian analysis finds Habelia and Sanctacaris Additionally, the probabilistic approach does not sup-
grouped in a clade at the base of Chelicerata (Fig. 5). port the monophyly of Hymenocarina and Megacheira.
AriaandCaronBMCEvolutionaryBiology (2017) 17:261 Page10of20
Fig.5MaximumcladecredibilitytreeofaBayesiananalysisofarthropodrelationships,usinganMkvmodelonamorphologicalmatrixof77taxa
and215characters.Habeliidansareinboldandred.Numbersnexttonodesareposteriorprobabilitieswhen<100
The critical uncertainties (e.g. presence of mandible) in by Tokummia and Branchiocaris [9], as well the detailed
the coding of large bivalved taxa related to protocaridids redescription of Waptia currently in progress, should
are likely responsible for the dissolution of Hymenocar- help clarify the validity of Hymenocarina as a clade.
ina compared to the parsimony-based topology, since The status of Megacheira is likewise dependent on
character state transformations are optimized differently the reevaluation of “multisegmented” forms such as
under a Bayesian treatment. The redescription of these Fortiforceps [4] with respect to the better-diagnosed
taxa in light of the new anatomical information provided Cheiromorpha [27].