exceptional variation on a common theme: the …...original scientific article exceptional variation...

ORIGINAL SCIENTIFIC ARTICLE

Exceptional Variation on a Common Theme The Evolutionof Crustacean Compound Eyes

Thomas W Cronin amp Megan L Porter

Published online 20 September 2008 Springer Science + Business Media LLC 2008

Abstract The Crustacea contain an amazing and often (tohumans) bizarre array of visual designs This diversityincludes many different examples of both simple andcompound eyes each with standard or uniquely crustaceanfeatures In this review we focus on the anatomicalvariation optical principles and molecular diversity ofcrustacean compound eyes to illustrate how the complicatedstructures involved in vision are adapted for particularenvironments Using this knowledge as a starting point andconsidering what is known of crustacean evolution overallwe present the most recent ideas of how crustaceancompound eyes have evolved and show how eyes that arebased on fundamentally different optical principles can infact be derived from each other and thus be closely relatedthrough common descent

Keywords Crustacea Compound eyes Apposition

Superposition Evolution Opsin

Introduction

The extant Crustacea contain six classes 42 orders 849families and somewhere over 52000 species (Martin andDavis 2001) Although they do not make up the mostspecies-rich group within the Arthropoda (the insects orhexapods do) the crustaceans exhibit as great a degree of

morphological diversity as is seen in any other animalphylum (Fig 1) This variability has led to a scientificfascination with understanding crustacean evolution As agroup the crustaceans have a predilection for marinehabitats although crustacean species can be found inalmost every conceivable type of habitat (eg coastalpelagic benthic and deep marine freshwater terrestrial)The wide range of light environments represented by thesediverse habitats has operated together with the overallmorphological diversity within the Crustacea to produce adizzying array of crustacean visual systems based on eyesranging from simple pigment cups to compound eyedesigns not seen in any other animal In this review wefocus on the evolution of compound eyes

No discussion of eye evolution is possible without ageneral understanding of the evolutionary history of thegroup of interest The crustaceans pose a particularlydifficult challenge in this regard however as there is somuch morphological diversity that it is difficult to charac-terize crustaceans with any single set of features andattempts at understanding their taxonomic groups andphylogenetic relationships based on morphology have beenproblematic for as long as they have been studiedFurthermore molecular studies have shown that theCrustacea are not a unified group but instead form severaldistinct lineages some of which are more closely related tothe insects than to other well-accepted crustacean lineages(Fig 1) While we recognize that our understanding of theevolution of Crustacea is far from complete we believe thata discussion of eye design from both anatomical andmolecular perspectives illustrates many key evolutionaryprinciples Within this review we highlight some of thetypical and unusual eye designs within the Crustacea anddiscuss their evolutionary implications

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T W Cronin () M L PorterDepartment of Biological SciencesUniversity of Maryland Baltimore County1000 Hilltop CircleBaltimore MD 21250 USAe-mail croninumbcedu

Basics of Compound Eyes

Almost every optical system known to exist in eyes can befound in one crustacean or another ranging through avariety of ldquosimplerdquo designs (eyes that have a single apertureand a retinal sheet) to a uniquely diverse set of compoundeye types (see Land 1984) While it seems certain thatsimple eyes arose independently several times in crustaceanevolution little is known about the evolutionary paths takento produce the very unusual assortment of simple eyedesigns present in modern crustaceans Most crustaceansthat have only simple eyes are small and unfamiliar as well

(see Fig 1) Consequently in this review of crustaceanvisual evolution we will restrict our discussion to thecompound eyes These are the designs used by all largewell-known crustaceansmdashlobsters shrimp crabsmdashas wellas by a vast diversity of crustaceans that are less familiar tomost of us but nevertheless successful and abundantanimals in their own right krill mysids water fleas andmantis shrimps for example It is also worth noting that thelargest diversity of compound-eye optical designs in anygroup of animals is found within the larger crustaceans (themalacostracans) particularly within the decapods (Fig 1)

The oldest eyes in the fossil record are compound eyesspecifically those of the trilobites While these are certainlyderived from earlier and simpler types that are lost to usand while trilobites are not thought to be ancestral to anymodern arthropods these eyes illustrate the common designfeatures on which todayrsquos compound eyes are based(Fig 2) The more fundamental trilobite design called theholochroal type (Clarke 1889) is thought to have operatedon the same principles of modern types found in todayrsquoscrabs butterflies and bees among other animals Hereeach fossilized preserved facet probably denoted a separateoptical unit called an ommatidium Ommatidia are theunitary elements of all compound eyes and in every caseextinct or modern contain a corneal lens some opticalstructures below it and a group of photoreceptors whichtypically function as a unit sampling one point in spaceTrilobite holochroal eyes have optics very much like thoseof modern nocturnal arthropods (Fordyce and Cronin1993) suggesting that these animals lived in dimly litwaters or were active only at night

Fig 2 The fossilized compound eye of the Devonian trilobite speciesPhacops rana Note the orderly rows of large lenses Unlike thecompound eyes of modern crustaceans in these early compound eyeseach corneal lens is thought to have served a miniature retina Theoverall image would have thus been formed from a mosaic ofminiature sub-images

Fig 1 Phylogenetic distribution of optical eye designs within themajor crustacean lineages Only the eye design of adults is indicatedDashed branches indicate lineages where compound eyes are onstalks Topology of the relationships drawn after Schram andKoenemann (2004)

464 Evo Edu Outreach (2008) 1463ndash475

The trilobite eye illustrated in Fig 2 displays a morecomplicated design called the schizochroal type (Clarke1889) Here each corneal lens seen on the surface formedan extended image using sophisticated optics and isthought to have served a small retina Neighboring facetsviewed adjacent regions of space so the visual world wasapparently sewn together from dozens of individual mosaicimages (Fordyce and Cronin 1989) The design seems tohave been ultimately unsuccessful and the trilobites thathad these eyes are long since extinct Distantly similareye designs exist today only in a few outlier species ofinsect larvae and some odd and rare insect parasites butnothing like schizochroal trilobite eyes ever appeared incrustaceans

Like the eyes of trilobites all modern compound eyesare built of repeated fundamentally similar ommatidialunits A compound eye can be considered to be a collectionof dozens to thousands of nearly identical units eachsampling the light of a small region of space for brightnessand often for color and polarization as well The entirevisual world is simply the sum of the points sampled by allthese ommatidia much like a digital image is simply a sumof the array of pixels within it Compound eye images aresometimes portrayed as multiple repeating views of thesame object (much like we see the world through amultifaceted prism) but in fact the overall view is formedin the same way as it is in our retinamdasheach visual unitcontributes to one point in the final image The questions tobe considered here are (1) how have these eyes evolved and(2) how are the compound eyes of modern crustaceansrelated to each other While general answers to these areclear the compound eyes we encounter today are so diversethat it is not yet possible to trace all the evolutionary pathsthey took to get to the present-day designs To get anappreciation of the diversity that must be explained wepresent some examples next

Crustacean Compound Eye Design

Sessile Apposition Eyes

The simplest optical design for a compound eye has eachcorneal facet devoted to a single photoreceptive rhabdommaking each unit or ommatidium a completely indepen-dent functional device The array of ommatidia determineshow the visual field is sampled and each ommatidium isisolated from its neighbors optically and frequently bypigment barriers as well This forms an appositioncompound eye the most common type found amongcrustaceans (and arthropods in general see Figs 1 3aand 4) In the simplest examples of this basic design theommatidial array sits on the ldquoheadrdquo of the crustacean as a

raised group of corneal facets Such eyes can be seen inmany isopods and amphipods for an amphipod examplesee Fig 4a from Talorchestia longicornis While theexternal organization of this eye is rather simple internallyit is quite specialized Eyes similar to these are found inmany small crustaceans although there are numerous minortaxa where compound eyes are lacking or where they have

Fig 3 Schematic diagrams of the three basic compound eye opticaldesigns found in crustaceans a apposition optics b refractingsuperposition optics c reflecting superposition optics Dashed greylines represent typical light paths through the crystalline cones to therhabdoms cc crystalline cone R rhabdom cz clear zone

Evo Edu Outreach (2008) 1463ndash475 465465

not yet been described (Cronin 1986 Porter and Cronin2008 see Fig 1)

The basic apposition design is often modified eithersubtly or radically in accordance with the lifestyles ofparticular organisms (see Nilsson 1989) For instance manylarval crustaceansmdashincluding all larvae of malacostracansmdashhave transparent apposition eyes wherein all the pigment isrestricted to the compact central retina (Fig 4b) Such eyesreduce the visibility of these otherwise transparent plank-ton A more profound modification is to collapse the retinainto a tiny blob of pigmented receptors and lead light fromthe very distant corneal facets to it via biological fiberoptics This can produce an eye with excellent visual acuityand rather good sensitivity that is simultaneously almost

invisible as in the deep-sea hyperiid amphipods (Land1989 see Fig 4c) In some small planktonic crustaceansincluding the famous ldquowater fleardquo Daphnia the twoapposition compound eyes are fused side-by-side to forma single spherical organ located under the animalrsquostransparent carapacemdasha ldquocompound-compound eyerdquo

Stalked Apposition Eyes

In most adult malacostracans that have apposition eyes theeyes no longer sit directly on the carapace and have insteadbecome mounted on stalks Placing a compound eye on astalk offers the advantage of an expanded visual field sincethe eye now can sit like a periscope away from its ownerrsquos

Fig 4 Examples of apposition or similar types of compound eyesfound in modern crustaceans a The sessile apposition compound eyeof the beach amphipod Talorchestia longicornis The eye is fixed tothe cuticle of the animal and each corneal facet seen in thephotograph sends light to a separate photoreceptive rhabdom (SeeFig 3a for schematic) b A zoeal larval stage of the mud crabRhithropanopeus harrisii showing its small and spherical appositioneye Many crustacean larvae have eyes similar to this c The doubleapposition eyes of the marine hyperiid amphipod Phronima seden-taria Each eye has two retinas visible as dark roughly bean-shapedpatches of pigment on each side of the lower part of the headPhotoreceptors in the upper retinas are fed by long fiber optics thatlead from corneal facets on the upper curved surfaces of the animalrsquos

head These retinas sample only a patch of light overhead probablysearching for objects forming shadows or silhouettes against the dimdown-welling light The lateral retinas sample space in the remainingparts of the visual field probably searching for bioluminescentobjects Photograph courtesy of T Frank Harbor Branch Oceano-graphic Institution dndashf The stalked apposition eyes of the fiddler crabUca tangeri showing how the eyes can be extended above theanimalrsquos body for a periscopic and panoramic view An overall viewof a female of this species is illustrated in d (photograph by F Fiol)while panels e and f show scanning electron micrographs of theommatidial array and the arrangement of the corneal facetsrespectively (photographs by J Jordatildeo)


carapace and the stalk provides the potential for mobilityof the eye as the animal or its visual targets move aboutThe eyes of fiddler crabs provide superb examples ofstalked ldquoperiscopicrdquo moveable eyes (Fig 4de)

Apposition eyes are optically the simplest of compoundeye designs and they tend to be less sensitive than othertypes As will be discussed later superposition eyes offerthe potential for greatly enhanced sensitivity Despite thisanimals like isopods and amphipods that live in the deepsea apparently have never evolved superposition compoundeyes and unlike all other deep-sea crustaceans (exceptpossibly some crabs) they continue to see through apposi-tion optics In some cases these eyes can achieveoutstanding sensitivity mostly by mating a relatively fewlarge corneal lenses with unusually short focal lengths to fatphotoreceptors (Land and Nilsson 2002 Nilsson andNilsson 1981) To achieve this elevated sensitivity howev-er the apposition eye design must decrease acuity as thelarge corneal lenses force a reduction in the total number ofommatidia

While they are optically the simplest of compound eyesapposition eyes potentially have one huge advantage overthe other designsmdashthey can subject different parts of thevisual field to different levels of inspection Because eachommatidium is an individual radiometer for its designatedspot in the visual field the axes of ommatidia can bealigned to be more closely parallel for more intensesampling of a given visual region or can diverge in regionsof lower resolution As a result an apposition eye can haveone or more patches of ommatidia designed to act like thefovea of a vertebrate eye These optical regions are usually

called ldquoacute zonesrdquo because they offer relatively acutevision For instance the tall eyes of fiddler crabs (Fig 4de)achieve elevated resolution near the horizon for samplingobjects in the flat worlds (eg sand flats) they inhabitFiddler crab eyes have numerous other specializations fortheir unusual lives reviewed by Zeil and Hemmi (2006)

Many other examples of visual field specializations canbe found among crustaceans with apposition compoundeyes but the most specialized eyes of all are found in thestomatopods or mantis shrimp Mantis shrimps separatedfrom other crustaceans hundreds of millions of years agoso their evolutionary adaptations have developed over trulydeep time Their eyes are so different from those of all othermodern animals and their early ancestors disappeared solong ago leaving only rudimentary fossils that it is difficultnow to reconstruct how their present complex forms aroseMantis shrimp ommatidia are built on a standard crustaceanplan with optics and anatomy much like what is seen inmany other species However the eye as a whole is dividedinto three distinct parts a dorsal region a ventral regionand an equatorial strip of ommatidia (see Fig 5) Theommatidia of the dorsal and ventral halves sample extendedvisual fields like any typical apposition eye with oneunusual aspect the visual fields of these two halves largelyoverlap so many points in the outside world are viewed byboth halves of the eye simultaneously Ommatidia in theequatorial strip typically arranged into six rows (butsometimes only two or three rows) have visual fields thatsample only a planar slice through visual space placedabout midway within the overlapping fields of thesurrounding ommatidia Thus within this plane single

Fig 5 The very unusual apposition compound eyes of stomatopodcrustaceans or mantis shrimps Panel a shows the tall eye ofLysiosquillina maculata while Panel b illustrates the more sphericallyshaped eye of Odontodactylus scyllarus In both species the eye isformed from three functional arrays of ommatidia the dorsal andventral hemisphere arrays and the midband array formed from sixparallel rows of ommatidia See the text for an explanation of howthese very unusual eyes function in vision The tall eye is well adaptedfor flat-world environments (much like the fiddler crab eye illustrated

in Fig 4dndashe) while the spherical eye is adapted to a more complexvisual environment such as might be found in a rubble field or on acoral reef Note the dark patches visible on parts of these eyes(particularly the right eye of L maculata) These indicate the patchesof ommatidia that receive light from the direction of the camera andare called lsquopseudopupilsrsquo The presence of three pseudopupils in asingle eye shows how the eye views a single point in space from threeindependent patches of ommatidia Photographs by RL Caldwell


locations in the external world are seen three times by thesame eye

This twisting and contorting of the eyersquos surface permitsa single eye to estimate the distance to any object in viewas long as it is not too far away Tall eyes like those inFig 5a do this with great accuracy in principle whileround mantis shrimp eyes (Fig 5b) are probably morelimited in the range to which they can carry out accuraterangefinding The equatorial strips of ommatidia arespecialized for high-quality color vision and for analyzingthe polarization of light Since these receptors view thecenter of the region of overlap a single point in space canbe analyzed simultaneously for form movement colordistance and polarization No other eye compound orotherwise is known to be capable of such high-qualityanalysis in parallel streams of visual information (Croninand Marshall 2001) By the way the ability of mantisshrimp eyes to analyze lightrsquos polarization might seemexotic but in fact most arthropods have this ability

Stomatopods have taken the apposition design just aboutto its limit and as might be expected their specializationshave an evolutionary cost Because only a tiny slice of thefield of view can be analyzed so thoroughly due to thetriply overlapping design the eye must constantly move tointegrate all possible aspects of visual information This ofcourse costs the animal time and must occasionally causethe mantis shrimp to miss seeing something importantespecially if the object is only briefly in view

Superposition Compound Eyes

Unlike apposition eyes in which each ommatidium is anindependent visual unit superposition compound eyes haveommatidia where the optics function cooperatively Groupsof corneal lenses focus light originating from a single pointin space onto a single rhabdom As in the apposition typeeach photoreceptor still views an assigned spatial locationand thus the density of sampling of the visual field remainsa function of the number of ommatidia But each rhabdomnow receives light through numerous different facets (seeFig 3bc) making for a much brighter image than isnormally possible using the apposition design Superposi-tion eyes have repeatedly evolved in both insects and incrustaceans and are thus taxonomically widespread (Landand Nilsson 2002 Nilsson 1989 see Fig 1)

Forming a superposition image is not optically straight-forward Single optical units in the cornea (typically joinedto crystalline cones) must redirect light not only the raysthat are axially aligned with the rhabdom (the onlyresponsibility of the lenses of an apposition eye) but alsoother rays entering the facet over a wide range of spatialangles All these rays must be correctly sent to rhabdomsmaking up a significant subset of the photoreceptor array If

this is done using refractive lenses (Fig 3b) by far the mostcommon optical devices used in living (and artificial)systems the image that is formed must be ldquoerectrdquo in otherwords the top of the image should correspond to the top ofthe focused object right must be to the right and so onThis is the precise opposite of an image formed by a typicallens as in a human eye which is always inverted andreversed

This paradoxical situation was resolved through theinsights of Sigmund Exner who published the first moderntreatise on compound eye physiology over a century ago(1891 a full English translation by RC Hardie wasreleased in 1989) The erect image is produced becausethe lensndashcone unit has an internal gradient of refractiveindex that is radially symmetrical around its long axis Theresulting bullet-shaped optic is called a ldquolens cylinderrdquoSuperposition eyes have another optical requirement theyneed to leave space inside the eyersquos volume to allow thecorrectly formed rays exiting the erecting lenses to have theopportunity to join with rays from other lenses arising fromthe same spatial location Thus a diagnostic feature of theanatomy of the superposition type is the presence of a gapor space between the superficial optical layer and thedeeper array of photoreceptive rhabdoms this is called theldquoclear zonerdquo (see Fig 3bc) Apposition eyes lack this zonebecause the rhabdoms invariably abut the terminations ofthe image-forming optics (or in the cases of appositioneyes with fiber optics the terminations of the light guides)

While they certainly can produce brighter retinalillumination superposition eyes do not offer the flexibilityof spatial sampling available to apposition eyes Becausethe various lenses must work together the eye cannot bedistorted or reshaped easily to form acute zones over-lapping visual fields or other types of specializations thatare frequently encountered in apposition eyes However theeye is not without recourse to some specialization Eyes ofeuphausiids (krill) and mysids form superposition imagesby refraction using lens cylinders and in shallow-livingspecies these eyes are usually spherical seeing aboutequally well in all directions In deep-sea species howeverthe superposition eye is very often formed into an hourglassor dumbbell shape (Fig 6) The upper half is expanded andflattened looking upward to produce a greatly enhancedsuperposition image of the dim light filtering down fromthe distant surface of the ocean This is joined at the equatorwith a more normal-looking lower half having a nearlyspherical field of view which is presumably devoted tosearching for bioluminescent flashes in other directionsAnother very unusually modified superposition eye existsin a mysid Dioptromysis paucinispinosa described byNilsson and Modlin (1994) Here most of the ommatidiaare arranged in the conventional spherical array but a singlecorneal facet near the margin of the eye is hugely enlarged


and is matched to a local retina of over 100 photoreceptorsApparently the optics of most of the original ommatidiahave been lost here leaving only a single optical unit ofcornea and crystalline cone forming a gigantic lens cylin-der Because erecting optics are present in the relativelyhuge corneal facet the retina here sees an erect imagewhich is greatly magnified compared to what is seen by therest of the ommatidial array It is thought that this miniaturetelescope in each eye is used to search for food or matesbut behavioral observations are thus far absent

The refracting superposition design is seen in insects aswell as crustaceans but crustaceans have evolved two othersuperposition designs rarely or never occurring anywhereelse Both of these use reflection of light rays either in partor wholly to form the superposition image The morewidespread of these designs is based entirely on reflectionfor image formation and is appropriately called thereflecting superposition eye (Fig 3c) This eye type isknown only for decapod crustaceans but it is fairlywidespread among them existing in almost every decapodorder (Fig 1 Porter and Cronin 2008)

Reflecting superposition seems out of the ordinary butin fact the principle is simple and straightforward Recallthat formation of a superposition image requires that lightrays be bent back towards the appropriate receptorEssentially this is what a mirror does it reflects rays backtowards their sources If two mirrors are mounted at 90deg toeach other they will form a completely upright image andif four mirrors are joined to form a long box with a squareopening any light ray entering the box from one end willbe reflected out the other end at an angle essentiallyidentical to that produced by refracting superposition

optics Notice that the light rays in Fig 3c follow verysimilar paths to those in Fig 3b even though the opticalmechanisms are quite distinct Biological mirrors areactually quite common and produce the eyeshine of manyanimals from shrimps and spiders to cats They are usuallybuilt of crystals of guanine or other reflective biologicalmaterial although many other means of reflecting light alsoexist see Land and Nilsson (2002) for other examples and avery readable account of mirrors in eyes The trick thatmakes reflecting superposition eyes work is the presence ofsquare corners in the corneal facets and in the mirror boxesbelow them Thus an immediate indication that a crusta-cean eye is of the reflecting superposition type is thepresence of square facets (see Fig 7 for an example from adecapod shrimp) The square facets in the eyes of lobstersare large enough to be seen (barely) without the aid of amicroscope

The third means of producing a superposition image wasworked out by Dan-Eric Nilsson of the University of Lundonly 20 years ago (Nilsson 1988) making it the mostrecently discovered biological image-producing systemNilsson terms this ldquoparabolic superpositionrdquo because thesides of the mirrors formed from the crystalline cones areshaped in the form of a parabola as seen in longitudinalsection The eye as a whole looks much like a refractingsuperposition eye having hexagonal facets and roughlybullet-shaped crystalline cones (like those in Fig 3b) butthere are no lens cylinders present The principle iscomplicated and Nilssonrsquos original paper (or Land andNilsson 2002) should be consulted for a full explanationbut the basic idea is that the corneal lenses focus lightrefractively and the beams entering the crystalline cone are

Fig 6 Double superposition compound eyes found in some deep-seaeuphausiid crustaceans (better known as lsquokrillrsquo) The euphausiids areone of the few crustacean groups containing refracting superpositioneyes with optics similar to the schematic in Fig 2b The eyes shownhere are rather unusual in that the dorsal half is arrayed so as to inspectjust the downwelling light arriving from the ocean above while theventral half forms a nearly complete spherical array sampling in allother directions These eyes are thus superposition analogues of the

fiber-optic eye type illustrated in Fig 4c a b Light-microscopic viewsof the double eye of Nematobrachion booumlpis (photographs by TFrank Harbor Branch Oceanographic Institution) c Scanning electronmicrograph of one double eye of Nematoscelis sp This eye hasbecome somewhat distorted during the preparation for imaging Theupper flattened array and the lower spherical array are easilydistinguished (photograph by D Pales)


redirected by the parabolic mirrors in the appropriatedirections to form a nearly perfect erect superpositionimage The design as a whole incorporates elements of bothrefracting and reflecting superposition optics (as well assome of the features of apposition eyes) and seems to havebeen an intermediate in the evolution of eyes in someanimals whose close ancestors use other optical principles

Evolution of Compound Eyes

Itrsquos obvious from the preceding discussion that crustaceancompound eyes come in a bewilderingly diverse set ofdesigns In addition the optical principles of one type maynot be easily compatible with those of a different design soit is often difficult to envision the intermediates that link thefully developed eye designs encountered in todayrsquos crusta-ceans For example it is not difficult to conceive how asessile compound eye can be altered into a stalked eye ofthe same basic design (say apposition) but it is moreproblematic to see the evolutionary route from apposition toreflecting superposition Making the problem more com-plicated optics and internal structures of fossil compoundeyes are usually difficultmdashif not impossiblemdashto work out(with trilobites as in Fig 2 being the exception) soreconstructing the operating principles of early compoundeyes is rarely practical

The best evidence available today to help us understandcrustacean compound-eye evolution comes from theirdevelopment The large and often optically complex eyesof adult stomatopods euphausiids and decapods almost all

originate from the much simpler apposition compound eyesof their larvae as in the transparent apposition eye of thecrab larva seen in Fig 4b (the only exceptions are speciesthat show direct development like crayfish) These eyes areoptically simple while being at the same time well designedfor the needs of larvae They are mostly transparent having acompact retina while providing panoramic coverage fororientation and for detection of oncoming predators (andperhaps for locating food as well) The apposition eyecontinues to function in many adult crustaceans like somecrabs which carry the larval plan through metamorphosisremodeling it by enlarging the eye and adding pigment andsupport

While the developmental path from a transparent appo-sition eye in the larva to any of the types of superpositioneye seems cryptic it turns out that larval eyes already havestructural features that are compatible with either apposi-tion refracting superposition or reflecting superpositionoptics in adults Nilsson (1983) noted that crustacean larvaleyes despite their fundamental apposition optics formsuperposition rays within the crystalline cones that are notused for image formation but that are readily adaptable foruse in the adult eye Thus the roots of both reflecting andrefracting superposition eyes reside in the larvae Theopposite transition can occur as well accounting for theappearance of apposition compound eyes in groups ofcrustaceans that normally possess only superposition eyesFor instance while decapod shrimps in general havereflecting superposition eyes as adults (eg Fig 7) adultshrimps of the family Spongicolidae may possess apposi-tion eyes produced by neoteny (Gaten 2007) Interestinglymysids brood their young so the juveniles are neverplanktonic yet developing mysids also have appositioncompound eyes that transform to refracting superpositioneyes in the adults (Nilsson et al 1986) Richter (2002) hasargued convincingly that paedomorphosis can account forthe appearances of unexpected compound eye types inadults of several crustacean taxa and he has presented arevised view of compound eye evolution incorporating thispremise

Paradoxically there is one group of crustaceans that doeshave apposition eyes both as larvae and as adults but wherethe larval retina is completely discarded at metamorphosisThis is the stomatopod crustaceans As noted abovestomatopods (mantis shrimps) have very unusual eyes withmultiple overlapping visual fields and subgroups ofreceptors specialized for different visual tasks Some ofthese specializations have involved fairly radical reorgani-zation of photoreceptors and oddly enough (and apparentlyuniquely for crustaceans) these receptors are constructedanew at the time of metamorphosis from larva to juvenile(see Cronin et al 1995 Cronin and Jinks 2001) Acomplete new retina forms alongside the larval one at this

Fig 7 The reflecting superposition eye of the grass shrimp Palae-monetes pugio Note the square facets easily visible on the surfacewhich are nearly diagnostic of this optical design (see Fig 3c for aschematic of reflecting optics)


time and in the newly molted juvenile a remnant of thelarval retina remains for a while but ultimately disappears(see Cronin and Jinks 2001 for a brief review and a list ofreferences)

The reason for this radical departure from crustaceanorthodoxy apparently can be traced to the extremelyunusual structures in the specialized rhabdoms that stoma-topods use to analyze the spectral content (or color) of lightThese photoreceptors are arranged into stacks or tiers suchthat light is sequentially absorbed in different parts of thespectrum as it passes through the entire length of the rhab-dom (see Cronin and Marshall 2004 for a review) Theunusual design is clearly a modification of the mostcommon crustacean plan where each rhabdom is formedfrom the fusion of typically eight receptor cells calledldquoretinular cellsrdquo In many crustaceans a short-wavelength-sensitive photoreceptor type called an R8 (meaningldquoretinular cell number 8rdquo) is placed on top of a group ofthe other seven cells R1ndash7 (see Fig 8 ldquoStep 1rdquo)Rhabdoms like this are found in all parts of mantis shrimpeyes that are not involved with color vision but ommatidiaspecialized to analyze color break up the R1ndash7 group intotwo subgroups placed on top of each other as in Fig 8ldquoStep 2rdquo This produces a three-tiered rhabdom with eachtier sampling a different part of the spectrum and theserhabdoms are devoted to shorter-wavelength regions oflight (violet through green) Apparently to improve thediscrimination of longer-wavelength light (yellow throughred) by stomatopods evolution has added colored filtersbetween the successive tiers of some classes of rhabdomsIn more primitive species one filter is added at the junction ofthe R8 cell and the divided group of R1ndash7 (Fig 8 ldquoStep 3rdquo)The species of mantis shrimps with the most complex eyes

have yet another filter at the junction between the twosubgroups of R1ndash7 as suggested by Fig 8 ldquoStep 4rdquo Thisprogression of complexity thus parallels stomatopod evolu-tion in general and ultimately leads to an extremelycomplicated but highly functional compound eye

A discussion of crustacean eye evolution would not becomplete without a brief reference to eyes that haveevolved in the opposite direction to those of mantisshrimps towards extreme simplicity Crustaceans inhabit-ing the deepest regions of the ocean and in particular theinhabitants of the hydrothermal vents of the mid-AtlanticRidge or the Galapagos Rift have often done away withoptics and separate ommatidia altogether forming the retinainto a thick sheet of photosensitive material with noremaining sign of its origin A good example of thisreduction is seen in the hydrothermal vent shrimps (VanDover et al 1989 Jinks et al 1998) where in some speciesthe retina has left the eyestalks entirely and migrated ontothe dorsal region of the carapace In the brachyuran ventcrab Bythograea thermydron larvae and postlarvae haveconventional apposition eyes but the eye regresses in theadults to form a nearly featureless mass of tissue containingthe visual pigment (Jinks et al 2002) These eyes are stillorgans of sight but they are no longer able to form imagesand instead are thought to act as anti-boil devicesresponsible for sighting the dim red light emitted fromthe hot water issuing from the vents

Molecular Evolution of Vision in Crustacea

As we have illustrated in the previous sections a con-siderable amount of research has been devoted to the

Fig 8 A series of schematicdiagrams to suggest the evolu-tion of complex photoreceptorsets in stomatopod crustaceans(mantis shrimp) The receptorarrangement illustrated in lsquoStep 1rsquois typical of that found in manycrustaceans as well as in someommatidia of mantis shrimpsThe other arrangements are foundonly in the stomatopods See thetext for an explanation of thefigure


evolution of crustacean visual system morphologies andstructures (also see reviews by Cronin 1986 2005) Theoptical structures and photoreceptors within the eye are alldesigned for the efficient capture of the light availablewithin a given habitat from the infrared of the deep-seavents to the full spectrum available to shallow coral reefdwellers At the foundation of any visual system howeverare the molecules responsible for absorbing photons of lightand converting this photic energy into a cellular signalRegardless of the overlying structure of the eye theunderlying light-capturing molecule is always a visualpigment composed of two parts a chromophore (vitaminA derivative) bound to an integral membrane protein(opsin) Visual pigments are characterized by the wave-length of light at which they absorb maximally Differentvisual pigments can be lsquotunedrsquo to different wavelengths oflight by the interaction between the chromophore andspecific amino acids within the opsin protein In the typicalcrustacean eye design the photoreceptor cells R1ndash7 have aspectral sensitivity in the blue-green range (around 500 nm)while the R8 cell has a spectral sensitivity in the violet toultraviolet range (see Fig 8 lsquoStep 1rsquo for photoreceptorschematic) these differences in sensitivity imply that eachphotoreceptor type expresses a different opsin forming aunique visual pigment However very few studies haveinvestigated the molecular evolution of crustacean visualsystems to explore how the evolution of the genesresponsible for vision (eg opsins) matches the evolutionof the structures in which they are found

If we look at the evolution of the available crustaceanopsin genes relative to the opsins known from the othermajor arthropod groups (eg insects and arachnids) severalimportant evolutionary patterns can be observed (Fig 9)With the interesting exception of opsin sequences frombrachyuran crabs all of the crustacean opsins form a singlesequence cluster This main crustacean cluster is mostclosely related to opsin sequences from insects (Hexapoda)and chelicerates (spiders and allies) that form visualpigments sensitive to longer wavelengths of light (generallygreater than 480 nm) So far although photoreceptorssensitive to violet and ultraviolet light have been physio-logically characterized in crustaceans (generally the R8cells) no full-length sequences of these shorter wavelengthopsins have been published yet Incomplete opsin sequen-ces thought to be from photopigments sensitive to bluewavelengths of light have been isolated from ostracods(Oakley and Huber 2004) Although the shorter lengthsof these sequences prevented us from including them in ourphylogenetic analyses their existence (in conjunction withthe placement of the main clade of crustacean opsins)suggests that arthropod visual systems evolved from anancestor containing at least two visual pigmentsmdashonesensitive to longer blue-green wavelengths of light and

another sensitive to shorter violet to ultraviolet wave-lengths of light

The only opsin sequences that donrsquot fall within the maincrustacean group are those from brachyuran crabs Al-though the eyes of brachyuran crabs are structurally similarto those of other closely related crustacean species theopsins contained within their photoreceptors are quiteunique relative to other characterized crustacean andarthropod sequences Furthermore the species that hasbeen described most completely Hemigrapsus sanguineusexpresses two distinct opsin sequences within the mainphotoreceptor (indicated in Fig 9 by triangles) Theexpression of two middle-wavelength opsin sequences hasalso been shown in a deep-sea species of lophogastridGnathophausia ingens Because the G ingens visualsystem lacks R8 cells (Frank et al 2008) it is assumedthat both of these opsins also are expressed in the mainphotoreceptor (Fig 9 indicated by squares) SimilarlyPenaeus monodon also appears to express two verydifferent opsin sequences (Fig 9 indicated by stars)although where these two opsins are expressed is unknownUnlike insects which appear to have a fairly well definedset of expressed opsins with each photoreceptor cellgenerally expressing a single opsin gene crustacean opsinsappear to be more lsquopromiscuousrsquo There is mountingevidence including the cases presented above and anothereven more extreme case in ostracods (Oakley and Huber2004) that the expression of multiple opsin genes in singlephotoreceptors is common in crustaceans

Summary

Within this review we have illustrated how the diversity ofanatomical forms that exists throughout the Crustacea ismatched by the optical structural and molecular diversitycontained within crustacean visual systems Although ourunderstanding of the evolution of this diversity is hamperedby our ever-shifting view of crustacean phylogenetic relation-ships several key ideas have emerged While there are anumber of crustacean groups with simple eyes or no eyes atall most crustacean lineages contain compound eyes withapposition optics Even those species with superposition eyesas adults have apposition eyes in larval forms indicating thatapposition eyes arose early within the crustaceans Superpo-sition eyes then represent a more derived eye type thatappears in three different crustacean groupsmdashthe decapodseuphausiids and mysidsmdashsuggesting at least two indepen-dent origins (Fig 1) Similarly crustaceans have put theireyes onto stalks multiple independent times suggesting thatthis is a visually advantageous arrangement

It is also apparent from looking at the distribution ofcompound eye types within the crustacean phylogeny that


Fig 9 Phylogeny of publicly available crustacean and selectedinvertebrate opsins based on maximum likelihood analyses of aminoacid residues The phylogeny was reconstructed using PHYML(Guindon and Gascuel 2003) and rooted (not shown) using bovinerhodopsin (NC_007320) chicken pinopsin (U15762) and humanmelatonin receptor 1A (NM_005958) and GPCR52 (NM_005684)Accession numbers are provided in parentheses behind each speciesname and the numbers above each branch indicate the bootstrap

proportion from 100 replicates (values less than 070 not shown) Thetaxonomic groups of major clusters of opsin sequences are indicatedThe division between opsins forming visual pigments with sensitivityto longer wavelengths of light (blue-green to red) versus shorterwavelengths of light (ultraviolet to blue) has also been designatedSpecies where more than one opsin sequence has been isolated areindicated by symbols stars = Penaeus monodon squares =Gnathophausia ingens and triangles = Hemigrapsus sanguineus


most of the diversity of optical designs is found in thelarger species In particular the decapods (crabs shrimpsand lobsters) exhibit all known optical types of crustaceaneyes including the reflecting and parabolic superpositiontypes not found in any other groups (Fig 1) This diversityin part reflects the large number of species within thedecapods as well as their ecological variability Howeverthis is not a complete explanation for the presence ofunique optical designs only within the decapods whichremains a puzzle to be solved

Finally there are many instances of convergence wheremultiple lineages have gained or lost traits independentlyAs just mentioned it is likely (although still open fordebate) that refracting superposition optics and the stalked-eye arrangement both evolved independently multipletimes Similarly a number of lineages have independentlylost eyes altogether Although based on different underlyingoptical types the eye designs of the hyperiid amphipodPhronima (Fig 4c) and the double-eyed euphausiids(Fig 6) and mysids (Gaten et al 2002)mdashwhich occupysimilar ecological environments in the deep seamdashillustratea functional convergence imposed by similar evolutionarypressures on the visual system to sample in differentdirections in space for different purposes

Significantly the phylogenetic relationships amongcrustaceans are still contentious particularly in comparisonwith the evolutionary relationships that are well docu-mented among most other modern animals A thoroughunderstanding of crustacean visual system evolution willbecome possible only with the establishment of a cohesivewell-supported crustacean phylogeny Correspondingly aswe move towards this goal a consideration of howcompound eyes arose and diversified will be an importantfacet for improving our understanding of crustaceanevolution The examples we have presented here representmany of the bewildering types of eyes found in thecrustaceans illustrating how fundamentally different opticalprinciples can be derived from each other and highlightingboth our current understanding of the evolution of thisvisual diversity and the mysteries that still remain to beuncovered

Acknowledgements This work was supported by grants from NSF(IOS-0721608) and AFOSR (02NL253)

References

Clarke JM The structure and development of the visual area in thetrilobite Phacops rana Green J Morphol 18892253ndash70doi101002jmor1050020203

Cronin TW Optical design and evolutionary adaptation in crustaceancompound eyes J Crustac Biol 198661ndash23 doi1023071547926

Cronin TW Invertebrate vision in water In Warrant E Nilsson D-Eeditors Invertebrate Vision Cambridge UK Cambridge Uni-versity Press 2005 p 211ndash49

Cronin TW Jinks RN Ontogeny of vision in marine crustaceans AmZool 2001411098ndash107 doi1016680003-1569(2001)041[1098OOVIMC]20CO2

Cronin TW Marshall NJ Parallel processing and image analysis in theeyes of mantis shrimps Biol Bull 2001200177ndash83 doi1023071543312

Cronin TW Marshall NJ The visual world of mantis shrimps InPrete FR editor Complex Worlds from Simpler NervousSystems Cambridge MA USA MIT Press 2004 p 239ndash68

Cronin TW Marshall NJ Caldwell RL Pales D Compound eyes andocular pigments of crustacean larvae (Stomatopoda and DecapodaBrachyura) Mar Freshwat Behav Physiol 199526219ndash31

Exner S The Physiology of the Compound Eyes of Insects andCrustaceans Translated from the German by RC Hardie (1989)republished by Springer Heidelberg 1891

Fordyce D Cronin TW Comparison of fossilized schizochroalcompound eyes of phacopid trilobites with eyes of modernmarine crustaceans and other arthropods J Crustac Biol 19899554ndash69 doi1023071548587

Fordyce D Cronin TW Trilobite vision a comparison of schizochroaland holochroal eyes with the compound eyes of modernarthropods Paleobiology 199319288ndash303

Frank TM Porter ML Cronin TW Spectral sensitivity visualpigments and screening pigments in two life history stages ofthe ontogenetic migrator Gnathophausia ingens J Mar BiolAssoc UK 2008 In press doi10107S0025315408002440

Gaten E Apposition compound eyes of Spongicoloides koehleri(Crustacea Spongicolidae) are derived by neoteny J Mar BiolAssoc U K 200787483ndash6 doi101017S002531540705597X

Gaten E Herring PJ Shelton PMJ Eye morphology and optics of thedouble-eyed mysid Euchaetomera typica Acta Zool 200283221ndash30 doi101046j1463-6395200200116x

Guindon S Gascuel O A simple fast and accurate algorithm toestimate large phylogenies by maximum likelihood Syst Biol200352696ndash704 doi10108010635150390235520

Jinks RN Battelle BA Herzog ED Kass L Renninger GHChamberlain SC Sensory adaptations in hydrothermal ventshrimps from the Mid-Atlantic Ridge Cah Biol Mar 199839309ndash12

Jinks RN Markley TL Taylor EE Perovich G Dittel AI EpifanioCE et al Adaptive visual metamorphosis in a deep-seahydrothermal vent crab Nature 200242068ndash70 doi101038nature01144

Land MF Crustacea In Ali MA editor Photoreception and Vision inInvertebrates New York Plenum Press 1984 p 401ndash38

Land MF The eyes of hyperiid amphipods relations of opticalstructure to depth J Comp Physiol [A] 1989164751ndash62 doi101007BF00616747

Land MF Nilsson DE Animal Eyes Oxford UK Oxford UniversityPress 2002

Martin JW Davis GE An updated classification of the recentCrustacea Science Series 39 Natural History Museum of LosAngeles County Los Angeles CA (USA) 2001 vii 123 pp

Nilsson DE Evolutionary links between apposition and superpositionoptics in crustacean eyes Nature 1983302818ndash21 doi101038302818a0

Nilsson DE A new type of imaging optics in compound eyes Nature198833276ndash8 doi101038332076a0

Nilsson DE Optics and evolution of the compound eye In HardieRC Stavenga DG editors Facets of Vision HeidelbergGermany Springer 1989 p 30ndash73

Nilsson DE Hallberg E Elofsson R The ontogenetic development ofrefracting superposition eyes in crustaceans transformation of


optical design Tissue Cell 198618509ndash19 doi1010160040-8166(86)90017-0

Nilsson DE Modlin RF A mysid shrimp carrying a pair of binocularsJ Exp Biol 1994189213ndash36

Nilsson DE Nilsson HL A crustacean compound eye adapted to lowlight intensities J Comp Physiol [A] 1981143503ndash10 doi101007BF00609917

Oakley TH Huber DR Differential expression of duplicated opsingenes in two eye types of ostracod crustaceans J Mol Evol200459239ndash49 doi101007s00239-004-2618-7

Porter ML Cronin TW A shrimprsquos eye view of evolution how usefulare visual characters in decapod phylogenetics Crustac Issues2008 In press

Richter S Evolution of optical design in the Malacostraca (Crustacea)In Wiese K editor The Crustacean Nervous System HeidelbergGermany Springer 2002 p 512ndash24

Schram FR Koenemann S Are the crustaceans monophyletic InCracraft J Donoghue MJ editors Assembling the Tree ofLife Oxford UK Oxford University Press 2004 p 319ndash29

Van Dover CL Szuts EZ Chamberlain SC Cann JR A novel eye inldquoeyelessrdquo shrimp from hydrothermal vents of the Mid-AtlanticRidge Nature 1989337458ndash60 doi101038337458a0

Zeil J Hemmi JM The visual ecology of fiddler crabs JComp Physiol [A] 20061921ndash25 doi101007s00359-005-0048-7


Exceptional Variation on a Common Theme The Evolution of Crustacean Compound Eyes

Abstract

Introduction








Summary

References


Almost every optical system known to exist in eyes can befound in one crustacean or another ranging through avariety of ldquosimplerdquo designs (eyes that have a single apertureand a retinal sheet) to a uniquely diverse set of compoundeye types (see Land 1984) While it seems certain thatsimple eyes arose independently several times in crustaceanevolution little is known about the evolutionary paths takento produce the very unusual assortment of simple eyedesigns present in modern crustaceans Most crustaceansthat have only simple eyes are small and unfamiliar as well

(see Fig 1) Consequently in this review of crustaceanvisual evolution we will restrict our discussion to thecompound eyes These are the designs used by all largewell-known crustaceansmdashlobsters shrimp crabsmdashas wellas by a vast diversity of crustaceans that are less familiar tomost of us but nevertheless successful and abundantanimals in their own right krill mysids water fleas andmantis shrimps for example It is also worth noting that thelargest diversity of compound-eye optical designs in anygroup of animals is found within the larger crustaceans (themalacostracans) particularly within the decapods (Fig 1)

The oldest eyes in the fossil record are compound eyesspecifically those of the trilobites While these are certainlyderived from earlier and simpler types that are lost to usand while trilobites are not thought to be ancestral to anymodern arthropods these eyes illustrate the common designfeatures on which todayrsquos compound eyes are based(Fig 2) The more fundamental trilobite design called theholochroal type (Clarke 1889) is thought to have operatedon the same principles of modern types found in todayrsquoscrabs butterflies and bees among other animals Hereeach fossilized preserved facet probably denoted a separateoptical unit called an ommatidium Ommatidia are theunitary elements of all compound eyes and in every caseextinct or modern contain a corneal lens some opticalstructures below it and a group of photoreceptors whichtypically function as a unit sampling one point in spaceTrilobite holochroal eyes have optics very much like thoseof modern nocturnal arthropods (Fordyce and Cronin1993) suggesting that these animals lived in dimly litwaters or were active only at night

Fig 2 The fossilized compound eye of the Devonian trilobite speciesPhacops rana Note the orderly rows of large lenses Unlike thecompound eyes of modern crustaceans in these early compound eyeseach corneal lens is thought to have served a miniature retina Theoverall image would have thus been formed from a mosaic ofminiature sub-images

Fig 1 Phylogenetic distribution of optical eye designs within themajor crustacean lineages Only the eye design of adults is indicatedDashed branches indicate lineages where compound eyes are onstalks Topology of the relationships drawn after Schram andKoenemann (2004)

































































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Abstract

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Summary

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Summary











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Abstract

Introduction








Summary

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Abstract

Introduction








Summary

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Abstract

Introduction








Summary

References

exceptional variation on a common theme: the …...original scientific article exceptional variation...

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