On the sighted ancestry of blindness – exceptionally preserved eyes of Mesozoic polychelidan ...

20 Pages·2016·8.3 MB·English

by  Denis Audo

Audoetal.ZoologicalLetters (2016) 2:13
DOI10.1186/s40851-016-0049-0
RESEARCH ARTICLE Open Access
–
On the sighted ancestry of blindness
exceptionally preserved eyes of Mesozoic
polychelidan lobsters
Denis Audo1,2* , Joachim T. Haug3, Carolin Haug3, Sylvain Charbonnier2, Günter Schweigert4,
Carsten H. G. Müller5 and Steffen Harzsch6
Abstract
Background: Modern representatives of Polychelida (Polychelidae) are considered to be entirely blind and have
largely reduced eyes, possibly as an adaptation to deep-sea environments. Fossil species of Polychelida, however,
appear to have well-developed compound eyes preserved as anterior bulges with distinct sculpturation.
Methods: Wedocumentedtheshapesandsizesofeyesandommatidiabaseduponexceptionallypreservedfossil
polychelidansfromBinton(Hettangian,United-Kingdom),Osteno(Sinemurian,Italy),PosidoniaShale(Toarcian,Germany),
LaVoulte-sur-Rhône(Callovian,France),andSolnhofen-typeplattenkalks(Kimmeridgian-Tithonian,Germany).Forpurposes
ofcomparison,sizesoftheeyesofseveralotherpolychelidanswithoutpreservedommatidiaweredocumented.Sizesof
ommatidiaandeyeswerestatisticallycomparedagainstcarapacelength,taxonomicgroup,andoutcrop.
Results:Ninespeciespossesseyeswithsquarefacets;Rosenfeldiaoppeli(Woodward,1866),however,displayshexagonal
facets.Thesizesofeyesandommatidiaareafunctionofcarapacelength.Nosignificantdifferenceswerediscerned
betweenpolychelidansfromdifferentoutcrops;Eryonidae,however,havesignificantlysmallereyesthanothergroups.
Discussion:Fossileyesbearingsquarefacetsaresimilartothereflectivesuperpositioneyesfoundinmanyextant
decapods. As such, they are the earliest example of superposition eyes. As reflective superposition is considered
plesiomorphic for Reptantia, this optic type was probably retained in Polychelida. The two smallest specimens, a
Palaeopentachelesroettenbacheri(Münster,1839)andaHellerocarisfalloti(VanStraelen,1923),areinterpretedas
juveniles. Both possess square-shaped facets, a typical post-larval feature. The eye morphology of these small
specimens, which are far smaller than many extant eryoneicus larvae, suggests that Jurassic polychelidans did
not developviagianteryoneicuslarvae.Incontrast,anotherspeciesweexamined,Rosenfeldiaoppeli(Woodward,1866)
,didnot possess square-shaped facets, but rather hexagonal ones, which suggests that this species did not
possess reflective superposition eyes. The hexagonal facets may indicate either another type of superposition
eye (refractive or parabolic superposition), or an apposition eye. As decapod larvae possess apposition eyes
with hexagonal facets, it is most parsimonious to consider eyes of R. oppeli as apposition eyes evolved through
paedomorphic heterochrony.
(Continuedonnextpage)
*Correspondence:[email protected];[email protected]
DenisAudoandJoachimT.Haugsharethefirstauthorship
CarstenH.G.MüllerandSteffenHarzschsharelastauthorship
1UniversitédeRennes1,EA7316,263AvenueduGénéralLeclercCS74205,
35042RennesCedex,France
2CentredeRecherchesurlaPaléobiodiversitéetlesPaléoenvironnements
(CR2P,UMR7207),Muséumnationald’Histoirenaturelle,Sorbonne
Universités,UPMC,CNRS,8rueBuffon,F-75005Paris,France
Fulllistofauthorinformationisavailableattheendofthearticle
©2016TheAuthor(s).OpenAccessThisarticleisdistributedunderthetermsoftheCreativeCommonsAttribution4.0
InternationalLicense(http://creativecommons.org/licenses/by/4.0/),whichpermitsunrestricteduse,distribution,and
reproductioninanymedium,providedyougiveappropriatecredittotheoriginalauthor(s)andthesource,providealinkto
theCreativeCommonslicense,andindicateifchangesweremade.TheCreativeCommonsPublicDomainDedicationwaiver
(http://creativecommons.org/publicdomain/zero/1.0/)appliestothedatamadeavailableinthisarticle,unlessotherwisestated.
Audoetal.ZoologicalLetters (2016) 2:13 Page2of20
(Continuedfrompreviouspage)
Conclusion: Polychelidan probably originally had reflective superposition. R. oppeli, however, probably gained
apposition eyes through paedomorphosis.
Keywords: Polychelida, Solnhofen, La Voulte-sur-Rhône, Osteno, Nusplingen, Posidonia Shale, Heterochrony,
Deep-sea adaptations, Superposition eyes
Background the cuticle became impregnated by calcium phosphate,
Eyesinthefossilrecord in a so-called Orsten-type preservation [18]. Among
The study of eye structures in fossil arthropods has fossilized arthropods, trilobites and Orsten crustaceans
long been limited to that of highly calcified trilobites share the advantage of being preserved extraordinarily
[1]. Due to their sturdy outer surface, eyes and interior well, retaining most of their original volume [18].
structures, such as substructures of the lenses, are Besides these early derivatives of different evolutionary
regularly preserved in trilobite fossils [2]. The investiga- lineages, fossilized eye structures of representatives of
tion of exceptionally well-preserved eye structures in extantgroupshavebeendescribedinOrsten-typepreser-
less heavily calcified arthropod taxa (e.g., crustaceans) vation, for example the compound eyes of an ostracod
has attracted a great deal of scientific attention in re- [19], an achelate phyllosoma larva [3] and a possible
cent years. Although the preservation of such an appar- maxillopod [17]. Eyes preserved uncompressed in three
ently fragile organ would appear to be exceptional, the dimensions, i.e. in their original volume, are also re-
preservation of eye structures in sclerotized arthropods ported in many arthropods from the La Voulte-sur-
is not uncommon. The good preservation of some such Rhône nodules, notably in thylacocephalans [20–24] and
fossil eyes has, in certain cases, even allowed the partial inglypheidlobsters[25].
reconstruction of putative optical properties [3–6]. A further source of exquisitely preserved fossils comes
Such studies focused on functional aspects of eyes pos- from the plattenkalks. Although the body volume of
sessed by early representatives of different arthropod these fossils was not preserved entirely, as for instance
lineages to infer possible ancestral features, and thus to in Orsten’s or La Voulte’s fossils, at least some speci-
shed light on the early evolution of eye structures in mens may show aspects of their original volume [26]),
sclerotized arthropods. These studies included eyes of or even appear almost uncompressed [27]. Specimens
presumably early chelicerates [7–11] which, however, with preserved eyes have been described from the fam-
have been alternatively interpreted as representatives of ous Solnhofen-type plattenkalks of southern Germany
the lineage towards Euarthropoda [12, 13] (see also (e.g. an isopod). Additional, although not very well-
Haug et al. critical review [9]). preservedexamplesoffossileyesincludethoseofbenthesi-
These early arthropods include a number of spec- cymid shrimps [28] and of cirolanid isopods [29, 30] from
tacular taxa, such as (1) Anomalocaris sp. from Emu theLateCretaceousSahelAlmaLagerstätte(Lebanon).
Bay Shale [4] which is one of the arthropods with the
highest known number of ommatidia in the compound Eyesinpolychelidanlobsters
eye, or (2) the early chelicerate Leanchoilia superlata Polychelidan lobsters are ascribed to Reptantia, a group
Walcott, 1912 which initially was believed to have pos- comprising mostly benthic crustaceans with elongated
sessed two pairs of compound eyes [14], but later was pleon, such as spiny, slipper or squat lobsters, cray-
suggested to have carried “just” one pair of bilobed fishes, hermit crabs, and true crabs. Among Reptantia,
compound eyes [10] (as do other species of Leanchoilia Polychelida is probably the sister group to Eureptantia
[15]). In addition, favorable incidents during fossilization comprising all remaining groups of Reptantia [31]. The
of Early Cambrian biota not only led to the preservation predominantly benthic polychelidans have retained
of prominent epidermal sense organs (e.g., compound some plesiomorphic characters from the ground pat-
eyes, cuticular sensilla), but also yielded information on tern of natantian shrimps, such as the triangular telson.
the anatomy, as was demonstrated most recently in the Polychelida is thus a key group for reconstructing char-
early sclerotized arthropod from Chengjiang Fuxian- acter evolution in Reptantia, and Decapoda as a whole.
huia protensa Hou, 1987, which displayed a tripartite Adults of extant species of Polychelida are all thought
brain and optic neuropil [16]. Further studies also in- to be blind and to inhabit deep-sea ecosystems [32].
cluded early representatives of the mandibulate lineage Their larvae, however, may retain functional eyes [33]
other than trilobites; i.e., softer (non-calcified) and which may degenerate over the course of development.
smaller fossils of early representatives Crustacea sensu In adults,the eyestalksare still present (exceptin Wille-
lato [17] discovered as uncompressed fossils. In these, moesiaGrote,1873),butthe corneaearealwaysreduced;
Audoetal.ZoologicalLetters (2016) 2:13 Page3of20
despite this, live specimens of Polycheles typhlops Heller, Württemberg, Germany) are parts of the Posidonia
1862 still reacted to the intensity of light [34]. However, Shale Formation. This formation represents a Fossil-
it is known that in the fossil record, many specimens of Lagerstätte celebrated for its exquisite preservation of an
polychelidan lobsters possessing eyes are present. Even abundant fauna of marine reptiles that included very
the oldest occurrence of fossil polychelidan, Coleia large specimens of ichthyosaurs, plesiosaurs, and croco-
uzume [35] from Japan and Tetrachela raiblana [36] diles. The Posidonia Shale Formation also yielded some
from Italy and Austria, both Carnian (Late Triassic), terrestrial tetrapods, numerous bony fishes, sharks, crus-
seem to have had developed eyes as, although the eyes taceans, crinoids attached to driftwood, ammonites, bra-
themselves may not have been preserved, their cara- chiopods, numerous bivalves and coleoids, including
pace margins are incised by developed ocular incisions some with soft parts preserved. Some plant fragments
[35, 36]. Despite being documented fossilized eyes have (in addition to driftwood) also occur [48]. Deposition of
not been sufficiently discussed in an evolutionary con- the Posidonia Shale and the nature of its palaeoenvir-
text [37–40]. Spence Bate [41] was the first to stress onment are subject of debate. Bottom water and/or
the occurrence of eyes in some fossil forms, and as- sediment seem to have been often anoxic, with short
sumed their reduction in extant species. More recently, period of oxygenation. The Posidonia Shale was pos-
Schweigert&Dietl[42]illustratedaneye-bearingspeci- sibly deposited at a depth of around 50–150 m [49].
men of Palaeopolycheles longipes (Fraas, 1855) from the The anoxia was possibly a result of significant product-
Nusplingen Plattenkalk and discussed its ommatidia. ivity in the overlying water, which may have caused the
On the basis of the ommatidial facets of Paleopopoly- benthic habitat to be quite dark.
cheles longipes [24] as reported by Schweigert & Dietl
[42], and its phylogenetic position, Ahyong [43] sug- Bajocian-Bathonian of Monte Fallano (Italy) Monte
gested that coleiids may have already shifted to deep Fallano is a recently discovered Fossil-Lagerstätte. Its
water, in which case the stem polychelids may have also flat-bedded, micritic limestones are similar to those of
evolvedindeephabitats. the plattenkalks of southern Germany; it was therefore
possibly deposited in a lagoon fringed by reefs in which
Palaeoenvironmentsandassociatedfaunas the (parautochthonous) fauna lived, similarly to the
younger southern German plattenkalks. This outcrop
Hettangian of Binton (United-Kingdom) The outcrop yielded terrestrial plants, insects, numerous fishes, in-
of Binton (Warwickshire, United-Kingdom) corresponds cludingcoral-feedingpycnodontsandcrustaceans [50].
to the Wilmcote Limestone member of the basal Blue
Lias Formation dating from Rhaetian to Hettangian. The Callovianof LaVoulte-sur-Rhône(France) The Fossil-
Blue Lias Formation was deposited in a shallow epicon- Lagerstätte of La Voulte-sur-Rhône is celebrated for its
tinental sea covering England, which was “normally no rich fauna preserving cephalopods with their soft parts,
morethanafewtensofmetersdeep”[44].TheBlueLias abundant ophiuroids, numerous thylacocephalans (with
Formationyielded otherfossils,includingichthyosaurs. huge eyes), numerous crustaceans, sea spiders, coela-
canths and sharks. The LaVoulte Lagerstätte is thought
Sinemurian of Osteno (Italy) The main outcrop is a to correspond to a deep-water environment, based upon
quarry along the lake Lugano (Ceresio), near Osteno vil- geological and palaeontological evidence (absence of
lage (Como, Italy). It is a Fossil-Lagerstätte (outcrop orientation of epizoans on sponges in adjacent outcrops,
with exceptional preservation of remains in connection, presence of deep-sea cephalopods) summarized in Char-
withfrequent soft-partpreservation).Ithasyieldedsome bonnier [22, 51]. Polychelidans were probably autoch-
terrestrial plants (allochthonous). It more importantly thonoustothisoutcrop[24].
yielded an important exceptionally preserved marine
fauna dominated by crustaceans and thylacocephalans, Kimmeridgian-Tithonian plattenkalks of southern
which also included fishes, cephalopods, polychaetes, Germany and Cerin (France) The southern Germany
and acorn worms [45, 46]. The palaeoenvironment is plattenkalks are among the most famous Fossil-
not well-constrained; however, Teruzzi [47] pointed out Lagerstätten. They areoftenreferredas“Solnhofen-type”
similarities in the sponge community with those devel- outcrops. They were deposited in the regressive trend of
oping at the limit between the modern neritic–pelagic the end of Jurassic in small lagoons. Cerin belonged to
basins. Osteno was therefore probably deposited in a the same palaeogeographic region [52]. These platten-
relativelydeeppalaeoenvironment. kalks preserved some terrestrial taxa with plants, insects
and tetrapods (e.g. Archaeopteryx) and a rich marine
Toarcian of Holzmaden and Gomaringen (Germany) fauna dominated by fishes and arthropods, and local
The outcrops of Holzmaden and Gomaringen (Baden- echinoderms, also including jellyfishes, brachiopods,
Audoetal.ZoologicalLetters (2016) 2:13 Page4of20
annelids, and acorn worms [53]. Most of the fauna was observations, we discuss the evolution of eye types and
probably parautochthonous to allochthonous, since optical mechanisms within Polychelida and propose new
traces oflifesuch asbioturbation,arerareinthese plat- ideasonthevisualecologyoffossilpolychelidans.
tenkalks. The plattenkalks were probably formed in a
quite shallow palaeoenvironment, ranging from 20 to Originofspecimens
60 m in depth [54]. In total, fourteen specimens of polychelidan lobsters with
distincteyestructuresandpreservedfacetswereexamined
Methods (Tables1and2):
Objectives
We present new data on eye structures of fossil Polyche- (1) a specimen ofColeia barrovensis M’Coy,1849
lida. This includes re-description of the specimen of from theHettangianofBinton(Warwickshire,
Palaeopolycheles longipes previously shown in Schwei- UnitedKingdom)preserving eyesand ommatidia,
gert & Dietl [42]. We also illustrate new specimens of firstobservedbyWoods[38]andwhichrepresents
Mesozoic Polychelida from Solnhofen-type plattenkalks theoldestfossilexaminedinthisstudy;
(Late Jurassic; Figs. 1 and 2), La Voulte-sur-Rhône (2) theholotypeofColeia vialliiPinna,1968from
(Middle Jurassic: Figs. 3, 4 and 5), and Gomaringen, theSinemurian (Early Jurassic)ofOsteno
Osteno and Binton (Early Jurassic: Fig. 6) and compare (northernItaly);
them to other fossil arthropods, whose living relatives (3) a specimen ofGabaleryonAudo etal.inpress
possesswell-developedeyes(Figs.7and8).Basedonthese from theToarcian (Early Jurassic)ofGomaringen
Fig.1LateJurassicPolychelidawithpreservedcompoundeyestructures.a-dPalaeopolycheleslongipes,SMNS63724.e-g.Knebeliatotoroi,
SMNS67916.h-k.Rosenfeldiaoppeli,SMNS66004.a.Presumedcompoundeyewithpartiallypreservedcornea.b.Detailofthecorneawith
squarefacets.c.SamedetailasinB;noteregularalignmentofsquarefacets,seeasterisks(*)indicatingeightfacetssurroundingacentralone.
d.Overviewimageofentirespecimen.e-g.Detailsofsquarecornealfacets,noteasterisk(*)markingsomefacetsinG.h.Presumedcompoundeye
withinpartpreservedcornea.i-j.Detailofcornealfacetswithapparentlyhexagonalprofile,noteasterisks(*)markingsomefacetsinJ,eachfacetis
surroundedbysixneighboredones.k.Overviewofentirespecimen.a-b,d,h-iarered-cyanstereoimages.Pleaseusered-cyanstereoglassestoview
Audoetal.ZoologicalLetters (2016) 2:13 Page5of20
Fig.2LateJurassicPolychelidawithpreservedcompoundeyes,continued.a.SpecimenofPalaeonpentachelesroettenbacheri(SMNS67903).
b.Close-uponrighteye.c.Close-uponfacettedregion.d.SamedetailsasC,noteasterisks(*)revealingeachsquarefacetbeingsurrounded
byeightneighboredfacets.Allimagesarefluorescencecompositeimages
(southwestern Germany).Thisspecimenistoo Plattenkalk (Germany) or two insects from the Early
poorly preservedtobeidentifiedtothe species level, CretaceousSantanaFormation(Brazil).
however,itisthefirstinwhich ommatidiaare For comparison purposes, we also documented 30
preserved[55]; additionalspecimensonwhicheyesarepreserved,butthe
(4–10)sevenspecimensfrom theCallovian outline of each ommatidium is not visible (see Table 3).
(MiddleJurassic)LaVoulte-sur-RhôneLagerstätte We additionally documented eyes of one isopod and in-
(France),amongwhichfourspecimens of sects that display preservation modes similar to those of
Proeryongiganteus[39],twospecimensof fossilpolychelidans.
Hellerocarisfalloti[39],andonespecimenof
Willemoesiocarisovalis [39];
(11–14) four specimens from the Late Jurassic Documentation
Solnhofen-type plattenkalks including one specimen Small specimens were documented utilizing composite
of Palaeopolycheles longipes and the holotype auto-fluorescence imaging [57–59], macro-fluorescence
of Knebelia totoroi Audo et al., 2014b, in which [58, 60] under polarized light (analyzed; [9, 10, 61–63])
preservation of ommatidia was previously reported by a single-lens reflex camera or a flatbed scanner.
by Audo et al. [56], the latter two from Nusplingen Composite images were processed in CombineZM/ZP,
(Late Kimmeridgian), a specimen ofRosenfeldia Zerene stacker, Microsoft Image Composite Editor or
oppeli (Woodward, 1866) from Sappenfeld near Photoshop CS3. For some specimens detailed close-ups
Eichstätt (Early Tithonian), and a small specimen of were documented with SEM (Jeol Neoscope 2 JCM
Palaeopentacheles roettenbacheri(Münster, 1839) 6000). Details of (isopod and insects) comparative ma-
from Eichstätt (Early Tithonian) (hencebeing the terial was documented on a Leica stereomicroscope or
youngest occurrences). Zeiss Axioskop 1 equipped with a Skopetek DCM 510
digital camera producing image stacks. Based on these
All of the above specimens are flattened to a variable image stacks, virtual surface reconstructions were calcu-
degree, including those from La Voulte which retained lated and presented as red-blue stereo anaglyphs accord-
most of their original volume. To assess the quality of ingtothemethodrecentlydescribedbyHaugetal.[64].
preservation, we compared our sampling of polychelidan
fossils with three specimens belonging to different
arthropod taxa, such as the isopod Palaega nusplingensis Calculationofeyeparameters
Polz, Schweigert & Maisch, 2006 from the Nusplingen Threevaluesweremeasuredonthehigh-resolutionimages:
Audoetal.ZoologicalLetters (2016) 2:13 Page6of20
Fig.3MiddleJurassic(Callovian)Polychelida(Proeryongiganteus)fromLaVoulte-sur-Rhône(France)displayingpreservedeyestructures.a-d.
SpecimenUJF-ID.11547.e-h.SpecimenUPMC-248.a,e.Presumedeyestructures.b-c,f-g.Detailsofsquarefacets,notethateachsquarefacet
issurroundedbyeightadjacentfacets,seeasterisks(*)inc(sameimageasb)andg(sameimagease).d,h.Overviewofentirespecimens
1. Eyediameter d;dueto theoftenincomplete in Table 2. For these specimens, mean value of
preservationand possibledeformationofthe eye, we ommatidia edge length was compared with other
assumed aroughlycirculardiameter. Wemeasured specimens. We note that the preservation of om-
thehighestdistance possible(axis)between two matidia varies. Some ommatidia appear convex,
opposingmarginsforeacheyes. Inthe caseofa others concave or surrounded by walls. These
more oval-shapedoutlinean averageofthetwoaxes variations, which may be linked to different
wasused. Inthe caseofincompletelypreservedeyes, preservation, may affect slightly the measurements
thegreatestmeasurablelength ontheeyewasused of ommatidia. This probable bias is unfortunately
(Tables1and3). unavoidable when dealing with fossil material, but
2. Either2a)the edgelengthofa square-shapedfacet considering the excellent preservation of measured
aor2b)thediameterofahexagonalfacet a,which ommatidia, this bias is probably limited.
equals 2×theedge length(Tables1,2and 3).Since 3. Thecarapacetotallength,measuredfrom themost
ommatidia edgelength isvariableacrosseyesurface, anteriortothemost posteriorpoint ofthe carapace,
we measured theedgelength ofasmany adjacent parallel tothe longitudinalaxis(Table3).
ommatidia aspossible and divided thisvaluebythe
numberofommatidia. Measurementsweremade The exact curvature of the eye surface cannot be
alongdifferentaxesoftheeyeandatdifferentplaces; measured, as all fossils showed a more or less strong
forallspecimens butthree (Table2),variationswere (although sometimes only a slight) compaction. To be
belowtheprecisionofourmeasurementorommatidia as cautious as possible, we considered both possible
were of similar sizes across the preserved portion of extreme shapes of an eye which may be either flat or
eye. The three specimens, in whichvariations in display a hemispherical outline. The original morpho-
ommatidia edge length were detected, are detailed logy most likely ranged somewhere between these
Audoetal.ZoologicalLetters (2016) 2:13 Page7of20
Fig.4MiddleJurassic(Callovian)Polychelida(Proeryongiganteus)fromLaVoulte-sur-Rhône(France)withpreservedeyestructures.a-g.Specimen
UJF-ID.14020.h-k.SpecimenFSL170603.a,h.Presumedremainsofcompoundeyes.b-e,i-j.Detailsofsquarefacets;notethateachsquarefacet
issurroundedbyeightneighborfacets,seeasterisks(*)ine(sameimageasd)andj(sameimageasi).f,g.Overviewofpartandcounterpart.
k.Overviewofentirespecimen
two extremes. In consequence, all further calculations Statistics
have to be considered estimations, and to refer only to To study the possible impact of palaeoenvironments and
the visible part of the preserved eye, which is the eye phylogenetic on eyes parameters, we performed a series
most likely formed more than a half sphere, i.e. almost of statistical analysis using R (http://www.R-project.org).
a full sphere; however we have no information on Measured values were first tested for normality (Shapiro
parts below the visible preserved parts. test) for whole samples(eye size, ommatidia)andinsub-
We then calculated how many ommatidia (n) are set defined by categories (familial assignment, outcrops);
present along the longest line across the surface by div- not allsubsetswere normallydistributed, for thisreason,
iding diameter (assuming a flat eye) or half circumfer- non-parametric tests (considered more robust for not
ence (πd/2 assuming a hemispherical eye) divided by normally distributed samples) were used for analysis of
(a). Based on this, the average opening angle for each the whole sample and a parametric test two compare
ommatidium was calculated as 180° divided by n (for normally distributed subsets (Coleiidae and Eryonidae
half sphere; opening angle for flat eyes is 0). The sur- ratios—see below; parametric tests are considered more
face of the eye was calculated as πd2/4 (flat) or πd2/2 valid when applied to normally distributed samples). We
(hemispherical). This value was divided by the surface compared the diameter of eyes to the carapace length to
of a single ommatidium (a2, for square-shaped; ((3√3)/ search possible link between the two variables (Spear-
2)(a/2)2, for hexagonal) to get the total number of om- man correlation). Subsequent test were based on the ra-
matidia per visible surface of the eye. tio “eye diameter” on “carapace length” and the possible
Audoetal.ZoologicalLetters (2016) 2:13 Page8of20
Fig.5MiddleJurassic(Callovian)PolychelidafromLaVoulte-sur-Rhône(France)withpreservedcompoundeyestructures,continued:Hellerocaris
fallotia-gandWillemoesicarisovalish-k.a-c.SpecimenMNHN.F.A50709,SEMimages(PhilippeLoubry).d-g.SpecimenFSL710108.h-k.Specimen
MNHN.F.A29521.a,d,h.Overviewofcompoundeyestructure.b,e-f,i-j.Detailsofsquarefacets,notethateachsquarefacetissurroundedby
eightneighborfacets,seeasterisks(*)inf(sameimagease)andj(partofi).c,g,k.Overviewofentirespecimens
influence of palaeoenvironments (outcrops) and phylo- Results
geny (familial assignment) (Kruskal-Wallis tests). Ratios Eyesandommatidia
of “eye diameter” to “carapace length” were compared All specimens examined possess anterior pairs of ball-
between Eryonidae and Coleiidae, since number of spec- or disk-shaped structures that strongly resemble stalked
imens for other families is not sufficient for statistical compound eyes of extant decapod taxa. On 14 speci-
analysis. Size of ommatidia was also compared to the mens,theseprotuberancesdisplayeithersquaredorhex-
diameter of the eyes. We used the square root of omma- agonal sculpturations. On the remaining specimens, the
tidia surface to normalize the size of ommatidia and preservation is not as fine, and these fine sculpturations
compare its variation to that of the diameter of the eye are not visible. The nature of sculpturations is slightly
(spearmancorrelation). obscured by compression in flattened specimens. How-
ever, objects with fragmentary volume preservation, as
for instance in specimens from LaVoulte, can be confi-
Phylogeneticcontext dently interpreted as fossilized compound eyes. Due to
Our evolutionary scenario is based on the phylogenies of the specific preservation of these eyes, some being partly
Scholtz & Richter [31] and Ahyong [43]. Familial assign- flattened, incomplete and/or not visible in their entirety,
ments follow Audo et al. [24], and Ahyong [43], except detailed descriptions are difficult. Ommatidia do usually
in the case of Rosenfeldia oppeli, which due to its un- not cover the entire surface. Therefore, the descriptions
usual appearance isnot consideredasaneryonid. are used as a basis for simple geometric assumptions
Audoetal.ZoologicalLetters (2016) 2:13 Page9of20
Fig.6EarlyJurassicPolychelidawithpreservedcompoundeyestructures.a-d.Gabaleryonsp.specimenSMNS67631fromtheToarcianof
Gomaringen.e-h.Coleiaviallii,holotypeMSNMi3368fromtheSinemurianofOsteno.i-j.Coleiabarrovensis,specimenNHMUK.I6589(photo©
NHMUK)fromtheHettangianofBinton.a,e,i.Overviewofpresumedcompoundeyestructures.b-c,f-g.Detailsofsquarefacets,notethateach
squarefacetissurroundedbyeightneighborfacets,seeasterisks(*)inc(sameimageasb)andg(sameimageasf).d,h,j.Overviewof
entirespecimens
and generalizations about the entire eye. Measurements 0.43). However, phylogenetic variations may help to ex-
and estimations of the properties of these eye structures plain differences in eyes proportion (Kruskal-Wallis χ2
aresummarizedinTable1,seealsoTable 2. =11.61; P<0.05). More precisely, representation of the
We find quite a variety of ommatidia sizes from 35– distribution of values for different families (Fig. 10)
90 μm, their inferred number also varies considerably; shows that: Coleiidae have in proportion larger eyes
depending on high or low estimation there are about than Eryonidae and that fossil species more closely re-
700–17.000to1500–34.000 ommatidia per eye. lated to themodern speciesofPolychelidae thanto fos-
sil species attributed to other families;
Differencesineyesizes
Comparison between the diameter of the eye and cara- – Palaeopentachelidaehaveinproportionlarger eyes
pace length shows that both values are linearly linked thanallother taxa(Notethatthisfamilyiscurrently
(Spearmann rho=0.80; P-value<10−9: Fig. 9). This sug- composedofa singlespecies:Palaeopentacheles
gests, as expected, that larger specimens have larger roettenbacheri);
eyes. – Eryonidae, stem-Polychelidaeand Rosenfeldia oppeli
Difference in the proportion of the eyes (diameter of haveeyesofsimilar proportions.
the eye=Eye Ø), relatively to the carapace length (CL)
cannot be explained by variations in palaeoenviron- We compared statistically Eryonidae to Coleiidae
ments based on our data (Kruskal-Wallis χ2=6.95; P= (sample-size for other subgroups – here families – is
Audoetal.ZoologicalLetters (2016) 2:13 Page10of20
Fig.7Comparisonwitheye-bearingarthropodsotherthanPolychelida:1.Isopoda.a,b.OverviewofspecimenofPalaeganusplingensisfrom
theNusplingenPlattenkalk,SMNS65512.Notethatthespecimenismainlyseenfromtheinside.c.Close-upofhead.d.Close-uponasmall
partofthecompoundeyeseenontheoutside.e.Close-uponleftsideofthehead,fromamoreobliqueanglethaninc.f.Close-upofhexagonal
facets.a,candearered-cyanstereo-images(usered-cyanstereoglasses)
insufficient). Eryonidae eyes are significantly smaller Discussion
than those of Coleiidae (Welch test: Df=30.8;P<0.01). Opticalmechanismsofcrustaceaneyesandinterpretation
offossilpolychelidaneyes
Ommatidialsize Generally, arthropod compound eyes have been classi-
Comparison between the square root of ommatidial fied to function according to two common optical prin-
surface and diameter of the eye shows that both values ciples: the ancestral apposition type and superposition
are linearly linked (Spearmann rho=0.87; P<10−4: type which most likely evolved several times in parallel.
Fig. 11). This implies that large eyes include larger om- In apposition eyes, every separate element of the com-
matidia. Ommatidia of La Voulte species (Fig. 11) are pound eye (ommatidium) acts as independent optical
generally slightly larger than other, unfortunately, our unit.Inthe different types ofsuperpositionthe cornea of
sample-size doesn’t allow for detailed comparisons be- each ommatidium may spread light onto photoreceptor
tween families or outcrops, so these differences cannot cells of adjacent ommatidia, thus forming a superim-
be distinguished from random variations. The small posed image. Apposition eyes are optimized for maximal
sample size and, as indicated above, variations in the optical resolution whereas superposition optics increase
preservation of ommatidia may also have obscured the absolute sensitivity of the eyes [65]. In modern crusta-
palaeoenvironmental signal. ceans, and specifically in decapods, a high diversity of