Contributions to Zoology, 67 (4) 223-235 (1998)

SPB Academic Publishing bv, Amsterdam

Optics and phylogeny: is there an insight? The evolution of superposition

eyes in the Decapoda (Crustacea)

Edward Gaten

Department of Biology, University’ ofLeicester, Leicester LEI 7RH, U.K. E-mail: [email protected]

Keywords: Compound eyes, superposition optics, adaptation, evolution, decapod crustaceans, phylogeny

Abstract cannot normally be predicted by external exami-

nation alone, and usually microscopic investiga-

This addresses the of structure and in paper use eye optics the tion of properly fixed optical elements is required construction of and crustacean phylogenies presents an hypoth- for a complete diagnosis. This largely rules out esis for the evolution of in the superposition eyes Decapoda, the use of fossil material in the based the of in comparatively on distribution eye types extant decapod fami- few lies. It that arthropodan specimens where the are is suggested reflecting superposition optics are eyes

symplesiomorphic for the Decapoda, having evolved only preserved (Glaessner, 1969), although the optics

once, probably in the Devonian. loss of Subsequent reflecting of some species of trilobite have been described has superposition optics occurred following the adoption of a (Clarkson & Levi-Setti, 1975). Also the require- new habitat (e.g. Aristeidae,Aeglidae) or by progenetic paedo- ment for good fixation and the fact that complete morphosis (Paguroidea, Eubrachyura). examination invariably involves the destruction

of the specimen means that museum collections Introduction rarely reveal enough information to define the

optics unequivocally. Where the optics of the

The is one of the compound eye most complex component parts of the eye are under investiga- and remarkable not on of its fixation organs, only account tion, specialised to preserve the refrac-

but also for the optical precision, diversity of tive properties must be used (Oaten, 1994). optical arrangements that have evolved. This is it is the However, perhaps response of the eye the particularly true of Crustacea, which includes to in adaptive pressures, resulting convergence, of nine out of the ten described examples types of that limits its usefulness in systematics. Particu-

compound eye (Nilsson, 1989). Such is the com- larly in those habitats where the effectiveness of plexity of the of most it is the is such in optics compound eyes, eye lessened, as deep-sea, cave- that likely once one had it would not be or evolved, dwelling burrowing crustaceans, the secondary another unless the latter bestowed a reduction replaced by or loss of the eyes that usually occurs is

It significant optical is for this reason and often advantage. unhelpful misleading. This leaves us that Land (1981) that structure with those animals suggested eye bearing highly-evolved eyes should be considered a conservative character. that be useful may in discussing evolutionary re- Given these facts, it might be that the Where expected lationships. similar advanced optics are functional of the used different morphology compound eye by groups of animals, it is tempting would be considered interested in the by anyone to assume that they are synapomorphies unless classification and of the Crustacea. there phylogeny are compelling reasons to think otherwise.

However, this is not the case for a number of This is not always true, and even at the phylum Most reasons. important from a practical point of similarities in level, eye structure may not always view is that the used optics by a compound eye be indicative of the phylogeny of the animals

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under consideration. The in both crusta- The main feature of the is presence superposition eye

ceans and insects of a compound eye containing that within the crystalline cone the light must be

the basic same structure has been considered one redirected across the optical axis of the ommatid-

of the most serious problems to anyone maintain- ium (Figs. 1C, E, G) to focus onto the target rhab-

ing the separate origins of these groups (Tiegs & dom. The different types of superposition eye are

Manton, 1958). If they are not monophyletic, it is defined by the way in which this redirection of

to this The is direct reflec- necessary explain phenomenon as ex- light occurs. simplest way by

detailed of the of the tion of incident the wall of the tremely convergence eyes rays at crystalline

crustacean and insect/myriapod groups. cone (Fig. 1C); this is the mechanism used in re-

In of such there be role spite problems may a flecting superposition eyes (Vogt, 1975; Land,

for the study of physiological optics in the con- 1976). It has been shown (Vogt, 1977) that focus-

struction of decapod phylogenies. Even though ing in this type of eye only works if the crystal-

the of modem such use techniques, as molecular line cones are square in cross section. Reflection

biology, numerical taxonomy, and cladistic analy- within such a “mirror box” redirects light across

the sis has increased in recent years, functional mor- optical axis, as can be seen when the cone is

phological descriptions remain the principal tool viewed from above (Fig. ID). A more complex

of the systematist. mechanism for redirecting light is seen in the

which refracting superposition eye (Exner, 1891)

utilises a continuous gradient of refractive index

Crustacean compound eyes within the cone (Figs. IE, F). The third mecha-

nism, termed parabolic superposition (Nilsson,

in all comeal Compound eyes are present crustacean 1988) uses a powerful lens, a cylindrical

classes and moveable stalked lens within the and except Copepoda, crystalline cone, a parabolic

eyes are present in the Malacostraca. In most reflecting surface at the cone wall (Figs. 1G, H).

these of the in xanthid crabs achieve cases, eyes are apposition type Some the same effect using

which the lens and with dioptric apparatus (corneal a crystalline cone a square cross-section,

crystalline cone) are in contact with the light-sen- rather than a cylindrical lens. A complete descrip-

sitive rhabdom (Fig. 1A). In this type of eye, light tion of the optical mechanisms involved can be

remains within a single ommatidium, passing found in Nilsson (1989).

from the corneal facet to the underlying rhabdom; The identification of the optics being used by

this results in reasonably high resolution but low any specimen is rarely straightforward, with the

In the sensitivity. the superposition eye (Fig. IB) the appearance of the comeal facetting only ex-

and the rhabdom dioptric apparatus layer are ternal evidence of optical type that can usually be

clear This The efficient of separated by an unpigmented zone. seen. most way packing cylindri-

in the of from cal ommatidia into is permits, theory, superposition light a hemispherical eye by us-

a number of corneal facets to 3000 in Ne- an in this the (up ing hexagonal array; way angular phrops norvegicus - Gaten, 1988) onto a single separation of the ommatidia is reduced to a mini-

in the and the resolution of the maximised. rhabdom, although practice superposition mum eye

focus covers several rhabdoms as a result of op- This is the situation used in apposition, refracting

tical aberrations. Even though the more periph- superposition and parabolic superposition eyes. eral of these facets contribute less the Where is in light to a square crystalline cone used, as

than the central there is still in- and image ones, an reflecting superposition eyes some parabolic

crease in of between 10 and 1000 sensitivity superposition eyes (Nilsson, 1988), a square

times over that of an apposition eye. This confers packing array will give optimum resolution. Plac-

considerable in much reliance a advantage low-light habitats, ing too on the external appearance

there is concomi- of the lead to For although not, necessarily, any cornea can problems. many

in the of the it assumed tant reduction resolution which eye years was that all eubrachyuran crabs

is capable (Land, 1984). used apposition optics as they possessed small.

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of the of Fig. 1. Diagrammatic representation main types crustacean compound eye: A, apposition eye, showing isolation of the

redirection of from the ommatidium; B, superposition eye, showing light many facets to the target rhabdom; C-H, light path through

viewed from the side and from above dotted line marks the ommatidial crystalline cones of superposition eyes (the axis); C, D,

reflecting superposition; E, F, refracting superposition; G, H, parabolic superposition. After Nilsson, 1990 (not to scale).

This not corrected the when the is hexagonally-faceted eyes. was eyeshine disappears eye exposed

until the of the to and also the direc- optics parabolic superposition eye light may vary according to

were correctly described (Nilsson, 1988). tion of observation (Exner, 1891; Shelton et al.,

In the of live specimens presence an eyeshine 1992; Gaten, 1994). Further identification of op-

caused tical that patch covering several facets, by a tapeta! type requires the eye be hemisected to

reflection from within the confirms that show the clear zone in that eye, superposition eyes or

superposition optics are in use (Kunze, 1979). the component parts of the eye are examined mi-

Care must be taken when using the absence of croscopically. Some information can be obtained

confirm the in from the of the eyeshine to optics as many species shape crystalline cone, but deter-

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initiation index the of the refractive profile of Very little work has been done on the develop-

crystalline cone using an interference microscope ment of superposition optics in the Decapoda.

be for between may necessary discriminating Nilsson (1983a) reported fundamental differences

optical types. between the optics of the crystalline cones from

the of furcilia larvae of the eyes euphausiid

Thysanoessa raschii and those from the 11th

Evolution and of larva of the development superposition stage decapod Macrobrachium rosen-

optics bergii. The refractive index distributions within

the crystalline cones were directly related to the

The evolution of from the superposition eyes ap- refracting and reflecting superposition optics

position eyes found in primitive crustaceans found, respectively, in the adults of these two

a The No poses particular problem. apposition eye species. differences, however, were found be-

inverted whereas produces multiple images in the tween the eyes of larval shrimps and larval crabs

a erect is these superposition eye single image present even though groups use different optics as

(Nilsson, 1989). To make this transition without adults. All described decapod larvae have trans- via intermediates going non-functioning requires parent apposition eyes distinguished from adult correction of the a continuing focusing properties apposition eyes by the absence of distal shielding of the that dioptric apparatus so light leaving the pigment between the crystalline cones. This is

crystalline cone is either afocal or is focused onto presumed to be an adaptation to increase camou- the rhabdom layer. In the reflecting superposition flage in the planktonic habitat of most larval

this correction is the comeal The isolation of the eye performed by decapods. necessary optical

lens, which becomes weaker as the ommatidium ommatidia is ensured by the relatively high, con-

and so the remain focused the stant refractive lengthens rays on index of the crystalline cones.

rhabdom In the (unpublished observations). re- Within an ommatidium, axial light is transmitted increase fracting superposition eye an in the re- to the rhabdom, whereas light from adjacent om-

fractive index of the proximal cone tip to effec- matidia is refracted away from the rhabdom and

second in tively form a lens results an afocal absorbed by the proximal shielding pigment beam leaving the crystalline cone in some insects (Nilsson, 1983a). This deflection of light in the

(Nilsson, 1989). The cone of the larval is similar the parabolic superposition eye crystalline eye to of (Nilsson, 1988) solves the problem light cross- mechanism used in the formation of the reflecting

ing the clear zone by using a light guide to trans- superposition image in the adult (Fig. 1C).

mit from the cone the rhab- The other essential feature of this of light crystalline to type eye

dom. is the of section development a square cross to

These fundamental differences in the way in the crystalline cone. This occurs gradually, start-

which this change from apposition to the different ing at the fifth postlarval moult in Palaemonetes

forms of superposition optics occurs means that varians (cf. Fincham, 1980). In species where the the latter are not always interchangeable. It ap- zoeal stages complete much of their development

to be to transform the pears theoretically possible within the egg (lecithotrophic, as opposed to

lens of the cylindrical parabolic superposition eye planktotrophic), the development of superposition

the into the continuous lens cylinder of refracting optics begins soon after hatching. These include

superposition eye (Nilsson, 1990). As various in- crayfish (Hafner et ah, 1982) and oplophorid termediates between the two types have been shrimps (Gaten & Herring, 1995). The develop- found it is that evolution of of very likely one type ment crystalline cones that are square in cross from the In in other has occurred. the case of the section occurs no species outside of the De- reflecting superposition eye, however, there is no capoda (except for some mayflies of the family

mechanism the used the of such apparent whereby optics Leptophlebiidae); indeed, presence a could have evolved from either of the other of types precise array square structures is extremely of in the animal This superposition eye. rare anywhere kingdom. sug-

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- Table I. The classification and those for which the is = Decapoda eye types. Only families eye type known are listed. Ap apposition,

= RS = refracting superposition, Mirror Para = Where the reflecting superposition, parabolic superposition. eye type is in parentheses, the is where type not certain; followedby another worker has found in the “/Ap”, apposition eyes same family.

Taxon Eye type Species Refs.

Suborder Dendrobranchiata

Superfamily Penaeoidea

Aristeidae RS Family Gennadus brevirostris Nilsson, 1990

Family Penaeidae Mirror Funchalia villosa Gaten, present study Superfamily Sergestoidea

Mirror Family Sergestidae SergestesSergesles spp. Welsh & Chace, 1938 Suborder Pleocyemata

Infraorder Caridea

Family Oplophoridae Mirror Oplophorus spinosus Land, 1976 Family Palaemonidae Mirror Macrobrachium sp. Nilsson, 1983b

Family Pandalidae Mirror Pandalus montagui M.L.M.L, Johnson, unpublished Family PasiphaeidaePasiphaeidae Mirror Parapasiphae sulcatifrons M.L. Johnson,unpublished Family Crangonidae Mirror Crangon crangon M.L, Johnson,unpublished Infraorder Astacidea

Family Nephropidae Mirror Nephrops norvégiensnorvegicus Gaten, 1988 Family Cambaridae Mirror Procambarus clarkii Tokarski & Hafner, 1984 Family Astacidae Mirror Family Astacus leptodactylusleptodactylus Vogt, 1975 Family Parastacidae Mirror Cherax Cherax destructor Bryceson & McIntyre, 1983 Infraorder Palinura

Palinuridae Mirror Family Panulirus argus Eguchi & Waterman, 1966

Infraorder Anomura

Superfamily Paguroidea

Family Diogenidae RS/Ap Dardanus megistos Nilsson, 1990 Family Paguridae Para/Ap Eupagurus bernhardus Nilsson, 1988 Superfamily Hippoidea

Family Hippidae (Ap) Hippa adactyla adactyla Gaten, present study Superfamily Galatheoidea

Family Aeglidae (Ap) iculata Aegla denticulatadent Gaten, present study Family Porcellanidae (Mirror) Porcellana platychelesplalycheles Fincham, 1988 Family Chirostylidae Mirror Chirostylus Chirostylus investigatoris Gaten, present study

Galatheidae Mirror Munida Family rugosa Gaten, 1994

Infraorder Brachyura

Section Podotremata

Family Dromiidae Mirror Dromia vulgaris Gaten, present study Mirror Family Homolidae ParamolaParamóla cuvieri Gaten, present study Family Raninidae (Mirror) Ranina raninaranina Gaten, present study Family Latreilliidae (Mirror) Latreillia eleganselegans Gaten, present study Section Heterotremata

Family Majidae Para Family Majidae Hyas sp. Nilsson, 1988

Family Portunidae Para Macropipus sp. Nilsson, 1988 Family Xanthidae Para/Ap Para/Ap Trapezia sp. Nilsson, 1988

Family Geryonidae (Ap) tridens (Ap) GeryonGetyon Gaten, present study Section Thoracotremata

Grapsidae Ap Hemigrapsus sanguineussanguineus Arikawa et al., 1987

gests that, whereas the evolution of cylindrical Distribution of eye types within the Decapoda lens is an uncommon it be systems not event, may the case that have reflecting superposition optics Apposition eyes are found in all the lower crus- evolved very rarely, perhaps only once. taceans that have compound eyes and in the lar-

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of all Previous based on structure val eyes decapods. They clearly represent phylogenies eye the symplesiomorphic condition, although the and optics

and of complex highly-evolved apposition eyes

Su- Detailed studies of and have been some crustaceans are certainly not primitive. eyes optics

used with success to elucidate of perposition eyes are only found in the Eumala- varying aspects of the decapod relationships. In a study costraca, with only refracting superposition eyes arrange-

- ment and connections of the - optic neuropiles, (Syncarida Anaspides: Peracarida Mysidacea: Elofsson & Dahl showed fundamental dif- - (1970) Eucarida Euphausiacea) found outside the

ferences between the malacostracan and non- Decapoda (Nilsson, 1989; 1990). malacostracan Work the eye. on photoreceptive

organs (including nauplius eyes) of lower crusta- An examination of those members of the De-

ceans has been used as evidence for four which been deter- higher capoda in the eye type has groupings of Crustacea: Malacostraca, Anostraca, mined (Table I) shows that all taxa except the Phyllopoda and Maxillopoda/Ostracoda (Elofs- Anomura and Brachyura predominantly use re- son, 1966). Dahl (1963) reviewed compound eye flecting superposition optics. The only exception structure with respect to the evolution of recent to this is the Aristeidae, which use refracting Crustacea. Based on a then comprehensive list of superposition optics (Nilsson, 1990). The Ano- both in- compound eye descriptions, including mura and Brachyura both contain animals using sects and crustaceans, Paulus (1979) argued in of apposition and various types superposition favour of the monophyletic origin of the Arthro- optics. The Anomura have reflecting superposi- poda. tion in the Galatheoidea the eyes (with exception in The discovery of a unique form of optics of the primitive Aeglidae) and either apposition, decapod crustaceans, termed reflecting superposi- refracting superposition or parabolic superposi- tion (Vogt, 1975), prompted a number of authors tion in the The to Paguroidea. Hippoidea appear to consider the relationships within the order in use apposition optics, although in common with the of this Land light discovery. (1981) came to the small. most burrowing forms, eyes are the conclusion that Euphausiidae were more In the Brachyura, the Podotremata have closely related to the Mysidae than to the Deca- to the square-faceted eyes although, prior present poda, based on the refracting superposition optics the of these eyes had not been de- study, optics shared these and that the by groups, suggested scribed. Based the examination of the of on eyes superorder Eucarida was unsound. He also three dromiid species (Dromia vulgaris, Crypto- grouped together the long-bodied decapods and dromia canaliculata and C. granulala) and one the galatheid anomurans as they were thought to homolid (Paramola cuvieri) there is little doubt be the only taxa sharing reflecting superposition that are used reflecting superposition optics constituted eyes. He concluded that eye design a within the Podotremata. All of these species have conservative character, providing a good indica- crystalline cones that are characteristic of this tion of evolutionary origins. Fincham (1980) optical type, flat-sided and square in cross-sec- came, independently, to much the same conclu- tion. The rhabdoms are of a typical superposition sions, but also included the Dromioidea and

there is an additional thin distal shape, although Homoloidea with the galatheids and long-bodied rhabdom across the clear zone. The extending forms as these groups also have square-faceted latter is noticeable in the of especially large eye eyes. The remaining taxa, Brachyura, Hippoidea Paramola cuvieri. The Heterotremata and Thora- and Paguroidea formed a second group, as they cotremata the use then assumed to retain (together forming Eubrachyura) were apposition eyes

in crabs parabolic superposition optics swimming throughout their adult life. These ideas were sup- and those whilst relying on concealment, other ported in general by Cronin (1986). All of the

shallow-water and terrestrial seemed to species, especially conclusions arrived at in these papers retain crabs, apposition optics. be reasonable, defining the cladistic proximity of

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the based observed groups on synapomorphies. are the penaeid shrimps of the family Aristeidae. The of subsequent descriptions refracting These use super- refracting superposition optics, al-

eyes from a of crustacean in position variety taxa some of the though species many crystalline

(Nilsson, 1990), however, cast considerable doubt cones are in squarish cross-section and are pack- on the of description refracting ed in a superposition square array over more than one third of

eyes as synapomorphic. the eye (Nilsson, 1990). This could indicate that

Further doubt on the use of in these optical types shrimps are changing from refracting to re-

phylogeny arose with the discovery that larval flecting optics, although the mechanism for such

are for decapod eyes pre-adapted the formation of a is unknown. change In addition, there is no

reflecting superposition (Nilsson, As known eyes 1983a). advantage in possessing refracting rather described above, the larval the func- than eye provides reflecting superposition optics in terms of tional basis for the reflecting mechanism as a either sensitivity or resolution. The situation seen of biproduct maintaining optical isolation of the in the Aristeidae indicate may a less direct trans- ommatidia in the transparent apposition As formation. Other into eye. shrimps moving deep seas, all decapod to be in this eyes appear pre-adapted such as the oplophorid Hymenodora glacialis, Nilsson way, (1983a) suggested that reflecting have abandoned reflecting superposition optics

superposition optics may have arisen more than the whole altogether, fdling eye with hypertro-

once. phied rhabdoms instead (Welsh & Chase, 1937).

Similarly, bresiliid shrimps have lost the crystal-

line cone found layer in the eyes of related Discussion shrimps, although the ommatidia still show signs

of in a being arranged square array, especially The use of descriptions of structure and the eye op- during postlarval stages (Gaten et al., 1998). tics may be of help in If constructing decapod the Aristeidae had abandoned reflecting optics

phylogenies as as attention is long paid to the after assuming a deep-sea existence and subse- restrictions alluded to above. If the stratigraphic quently moved back to a brighter habitat, they

of the extant crustaceans ranges decapod (exclud- would then need to evolve a suitable optical ar- those with reduced absent ing or eyes) is com- rangement. The evolution of graded-index crys- bined known with the optical a number of talline rather than types, cones, crystalline cones with a

patterns are apparent 2). The extant Penaei- (Fig. square cross-section, would now result in refract-

dea, Caridea, Palinura and Astacidea all possess ing superposition optics (Nilsson, 1990). reflecting superposition These (with In eyes. groups contrast to the relative predictability of the the of the possible exception Penaeidea) probably long-bodied decapods, the Anomura and Brach- arose from an explosive radiation in the Devonian yura include species using apposition optics and and Carboniferous (Hessler, 1983) from an ances- all three types of superposition optics. The situa- tor that may have possessed reflecting superposi- tion is further confused by the variety of special- tion eyes. Although reflecting optics could have ised habitats occupied by the adults of these evolved in each of independently these taxa, there infraorders, often in resulting convergent evolu- is evidence no to that this was the case. tion. suggest Deep-sea forms such as the Homolodromii- assumed If it is that this state was to all common dae, Homolidae, Latreillidae, Cymonomidae, and ofthe it is early Decapoda, only necessary to some Xanthidae sug- Majidae, and Portunidae, are that gest these unusual optics evolved once from to thought show signs of regressive evolution the apposition eyes of the ancestral eumalacostra- brought about by the uniform conditions of this can. Accurate of descriptions the facet patterns in habitat. These adaptations are said to include un- fossil decapod eyes may well provide an answer of the reduction rolling abdomen, of the eyes and to this question. the of weakening the locomotor system (Stevcic, The only long-bodied decapods using super- evolution 1971). Similarly, regressive may occur position optics that are not of the in reflecting type burrowing species (such as the brachyurans

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Ranina and and the retention of the larval Corystes, anomurans Hippa apposition eye was neces-

and reduction of the before this habitat could be Albunea), again leading to a sary exploited.

eyes. According to Fincham (1980) burrowing None of the Paguroidea possess square-faceted

members of the superfamily Thalassinoidea also eyes. Some Paguridae have parabolic superposi-

In have small, hexagonally-faceted eyes. species tion eyes (Nilsson, 1988), whereas refracting su-

from such stable environments, especially the perposition eyes have been described from two

it is often difficult dis- of and deep seas, particularly to species Diogenidae (Nilsson, 1990) most

tinguish adaptive from ancestral features. Some of the smaller hermit crabs of both families have

taxa exhibit a progressive loss of optical function apposition eyes. It is proposed here that the Pagu-

with the from depth, as seen in galatheid genus Muni- roidea arose square-faceted ancestors, prob-

in dopsis (Zharkova, 1975) and the brachyuran ably evolving apposition eyes initially. This evo-

Cymonomus (Rice, 1990). lution from using superposition optics to using

Within the Anomura, there is a distinction be- apposition optics would be the reverse of the

tween the Galatheoidea, which mainly have usual situation where animals with superposition

facets and and the evolve from the square use reflecting optics, optics plesiomorphic apposition

Paguroidea (and probably the Hippoidea), which state. Migration of an ancestor with superposition

would do not. Reflecting superposition optics are used eyes into a bright habitat not necessarily

within the Galatheidae (Gaten, 1994), although lead to the abandonment of superposition optics.

the differ somewhat from the insects eyes those of long- Some day-flying have superposition eyes bodied decapods because they use a rhabdomeric that approach the theoretical limit of resolution

to channel axial from the for It is also light guide light crystal- compound eyes (Land, 1984). un-

the line cones to the rhabdom layer (Gaten, 1990). likely that each step in the evolution of super-

be in Based only on an external examination, the eyes position eye could reversed such a way that of Chirostylidae also appear to use reflecting a typical apposition eye would be the end prod-

The situation For these it is assumed that the optics (unpublished observations). uct. reasons, ap-

in the Porcellanidae is not quite so clear. Al- position eye found in some pagurids is the result

much of the is covered with of though eye square progenetic paedomorphosis, with the apposi-

facets, the crystalline cones are frequently round- tion optics found in the larvae retained in the ed at the corners, leading Fincham (1988) to con- adults. Paedomorphosis is probably a common

clude that reflecting superposition optics could occurrence in the unstable inshore environment

only be used over part of the eye. It may be that and has been implicated in the evolution of many

in the of porcellanid eyes are process developing, crustacean orders (Schram, 1982). Subsequent

of The the of or losing, this type optics. Aeglidae are movement the adults to deeper water, or a

& darker would the most primitive galatheoids (Martin Abele, habitat, inevitably lead to evo-

It 1986) and are the only galatheoids having hexa- lution of a more sensitive eye. might be ex-

gonally-faceted eyes. They are also the only ano- pected that reflecting superposition optics would

murans endemic to South America and the only evolve as the larval decapod eye is preadapted for

freshwater of the infraorder. In the evolution of this of representatives type eye. However, as

view of the isolated of this and position group (both only parabolic refracting superposition eyes

and it is found in this this be indicative biogeographically ecologically) not easy are group, may

to explain the evolution of aeglid optics. How- that optics of these types evolve more readily

have terrestrial ever, they may evolved from a than that found in reflecting superposition eyes.

& and the loss of The be divided into fol- ancestor (Martin Abele, 1986) Brachyura may groups reflecting superposition optics, if they ever pos- lowing two optical strategies along much the

sessed them, may have been concerned with this same lines as the Anomura. The primitive crabs

in As the stage their evolution. no crustacean with within families Dromiidae and Homolidae

this of type eye has made the transition to a ter- (and probably Raninidae and Latreilliidae) all

restrial of life it way may be that the neotenic have square-faceted eyes and crystalline cones

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Fig. 2. The of the crustaceans those with reduced stratigraphic ranges extant (excluding or absent eyes) together with the optics used

(in parentheses where The dotted lines indicate presumed). possible evolutionary relationships (based on Schram, 1982;Wagele, 1989; Glaessner, 1969).

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the larval decapods and ancestral crustaceans is

symplesiomorphic, as detailed above. Animals

in- moving to a light-deprived environment must

of the and one of crease the sensitivity eye way

doing this, in the short term, is to increase the size

of the ommatidia. This results in a larger aper-

ture, admitting more photons, and a longer rhab-

When dom, which is able to absorb more photons.

reaches certain size and the sides of the the eye a

crystalline cone are angled appropriately, super-

facets can occur in position of rays from several Fig. 3. Diagram illustrating the suggested steps in the evolution At this the the dark-adapted eye (Fig. 3b). stage, of the reflecting superposition eye: a, apposition eye focusing

into the will still retain thin axial light and redirecting non-axial light shielding pig- eye a long, apposition-type

increase the ment; b, in order to sensitivity, shielding pigment rhabdom. To take advantage of the light available

retreats of proximally, ultimately allowing superposition par- formation of at the point of superposition, the a axial from the rhabdom ex- rays adjacent facets; c, proximal be more bulky proximal rhabdom would expected pands to take advantage of the superposed light; d, the distal thin rhabdom would remain of the although a crossing rhabdomeric light guides are replaced by extensions the clear This in the situ- crystalline cone cells (not to scale). zone (Fig. 3c). is, fact,

ation found in the Galatheoidea and the Podotre-

with flat sides typical of those using reflecting mata, and also in those Paguroidea and Brachyura

In superposition optics. In contrast, no members of that use parabolic superposition optics. those

the this combination of fea- where migrations Eubrachyura possess species, screening pigment

tures. The status of the former families is the transform the optics from superposition to appo-

distal rhabdoms would be useful subject of regular rearrangement with one or sition, the thin

and for across the clear zone more routinely removed from the Brachyura transporting light (D.-E.

sometimes reassigned to the Anomura (see refer- Nilsson, personal communication). However, in

The of those superposition optics at all ences in Abele, 1991). presence reflecting species using

times aristeid and optics in these families, and in no other brach- (such as oplophorid shrimps)

to lend to the the of in the clear zone will yurans, would seem some support presence light guides the concept of the taxon Podotremata (Guinot, 1977). reduce the resolution and contrast sensitivity

that of However, as it is suggested here this type of the eye, due to the absorption photons by

rhabdoms. where the is of optics is symplesiomorphic for the Decapoda, non-target In eyes image in this the of the its possession would not imply a phylogenetic degraded way, replacement

rhabdomeric with cone grouping. light guides crystalline This One unusual feature of the dromiid and homo- extensions should result in a sharper image.

of thin rhab- would lead to the situation found in most of the lid eyes examined is the presence a

zone 3d). If the domeric light guide that crosses the clear to long-bodied decapods (Fig. sequence

of events the of link the crystalline cone stalk and the proximal was as suggested here, possession would be indicative of fusiform rhabdom. This feature is similar to that a rhabdomeric light guide

than and a more rather a seen in the eyes of galatheids (Gaten, 1994) primitive eye constituting

in those taxa with in the porcellanid anomurans (Eguchi et ah, synapomorphy. Similarly, eyes

have 1982). If the possession of such light guides con- in which the crystalline cone extensions re-

the of the the Caridea and stituted a synapomorphy, then optics placed light guides (Penaeidea,

this situation is to be the Galatheoidea and the Podotremata might be re- Astacidea), presumed

How- result of It must be that garded as evidence of a common ancestry. convergence. emphasised

it is here that this of is the here is ever, suggested type eye evolutionary sequence suggested

of a more primitive design than that seen in other largely speculative.

found in The decapods. The apposition eye (Fig. 3a) remaining Brachyura possess apposition

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or The eyes parabolic superposition eyes. pres-

of is ence apposition eyes once again assumed to be a result of progenetic paedomorphosis in the

shallow seas (Gould, 1977) during the adaptive

radiation of the Eubrachyura in the Upper Creta-

ceous 1980). A number of (Glaessner, sugges- tions have been proposed for the origin of the

Brachyura (see Stevcic, 1971) although all of these consider the Podotremata to be the most primitive crabs. Based on a consideration of the

optics alone, there is no reason to suggest that the

higher crabs evolved from the Podotremata rather

than from of the extant infraorders. The any ap-

found in adult crabs is position eye some simply

a version of the in larger, stronger eye seen all decapod larvae, but with the addition of distal pigment around the crystalline cones (Land,

1981). The subsequent evolution of superposition optics would not be unexpected in those crabs 4. the Fig. Dendrogram illustrating presence of reflecting moving to a darker habitat. However, one of the superposition eyes throughout the Decapoda and the presumed main reasons for that super- loss suggesting reflecting of these optics in some taxa. Groups not shown are all

have evolved once is the to The is based position optics only fact thought use apposition optics. phylogeny on that in the all Burkenroad (1963), modified according to Fincham (1980) and Eubrachyura superposition eyes are Martin & Abele of the that (1986). parabolic type. Given the larval deca-

is for the evolution of reflect- pod eye preadapted

ing optics (Nilsson, 1983) it might be expected that this of would have evolved in the the of type optics occurrence refracting superposition eyes higher crabs. The fact that have must be considered to be result of they parabolic a convergence indicate that superposition eyes may reflecting as they have evolved independently several times

do not and that in insects optics readily evolve, perhaps and probably four or five times in the have evolved they only once. Crustacea. Reflecting superposition optics evolv-

ed (possibly only once) in the early decapods and

are retained in almost all extant long-bodied

Conclusions in decapods, the galatheoid anomurans and in the

Podotremata (Fig. 4). It is suggested here that the It is neither nor desirable to to con- loss of has possible try reflecting optics occurred a number of

a realistic based on a times in the struct phylogeny single Decapoda, probably following migra-

character. occurs too in com- tion to habitat Adaptation readily a new (Aristeidae), or by proge- that pound eyes to be sure similarities are not due netic paedomorphosis (Paguroidea and Eubrach-

to In of such solely convergence. spite complica- yura). Subsequent evolution of parabolic and re-

some valuable information can be obtained tions, fracting superposition optics has occurred in from the of and should these result study compound eyes they groups as a of moving to a darker be considered in the construction of habitat. any decapod phylogeny. In view of the evolutionary sequence suggested

The ancestral eumalacostracan have that must had here, apposition eyes have led to superposi-

in common with all lower tion apposition eyes, crus- eyes and then reappeared before evolving taceans. As apposition also occur as a result into other of the eyes types superposition eyes, inevi- of their in heterochrony, presence any taxon can table conclusion is that the study of optics alone have little will phylogenetic significance. Similarly, solve very few phylogenetic problems.

Downloaded from Brill.com10/11/2021 08:33:28AM via free access - 234 E. Gaten Evolution of superposition eyes in Decapoda

Acknowledgements Fincham, A. A., 1980. Eyes and classification of malaco-

stracan crustaceans. Nature, 287: 729-731.

Fincham, A. A., 1988. Ontogeny of anomuran eyes. Symp I would like to thank Drs. A. L. Rice, P, J. Herring and M. H. Zool. Soc., 59: 123-155. Thurston (Institute of Oceanographic Sciences) and Mr. P. 1988. the Gaten, E., Light-induced damage to dioptric appa- Clark (The Natural History Museum) for access to their ratus in Nephrops norvegicus and the quantitative assess- collectionsof Crustacea. Dr. P. J. Hogarth (Departmentof Biol- ment ofthe damage. Mar. Behav. Physiol., 13: 169-183. ogy, University of York) generously donated the eyes of 1990. The of Gaten, E., ultrastructure of the compound eye dromiid crabs, and Mr. D. Bova (Scottish Office Agriculture Munida and rugosa (Crustacea: Anomura) pigment migra- and Fisheries Division) kindly supplied some other specimens. tion during light and dark adaptation. J. Morphol., 205: My thanks are due also to Dr. P. M. J. Shelton and Magnus 243-253. Johnson (Department of Biology, University of Leicester) for Gaten, E., 1994. Geometrical optics of a galatheid compound their critical comments on the manuscript. Finally, I would like eye. J. comp. Physiol., (A) 175: 749-759. to thank Professor D.-E. Nilsson (Department of Zoology, Gaten, E. & P. J. Herring, 1995. The morphology of the re- for discus- University of Lund) a most helpful and stimulating of larval flecting superposition eyes oplophorid shrimps. sion about the evolution of crustacean optics. J. Morphol., 255: 19-29.

Gaten, E., P. J. Herring, P. M. J. Shelton.& M. L. Johnson,

1998. of the of Comparative morphology eyes postlarval References bresiliid shrimps obtained from the region of hydrother-

mal Biol. Bull. In vents. press.

Abcle, L, G., 1991. of and mo- Comparison morphological Glaessner, M. F., 1969. Decapoda. In: R. C. Moore (ed.), lecularphytogeny of the Decapoda. Mem. Queensl. Mus., Treatise on invertebrate paleontology: 339-533 (Kansas

31; 101-108. Univ. Press, Lawrence). Arikawa, K., K. Kawamata, T. Suzuki & E. Eguchi, 1987. Glaessner, M. F., 1980. New Cretaceous and Tertiary crabs of function and Daily changes structure, rhodopsin con- (Crustacea: Brachyura) from Australia and New Zealand.

in the of the crab tent compound eye Hemigrapsus san- Trans. Roy. Soc. South Aust., 104: 171-192. guineus. J. Physiol., 161: 161-174. comp. (A) Gould, S. J., 1977. Ontogeny and phylogeny: 1-501 (Belknap

K. P. & P. 1983. quality and ac- Bryceson, McIntyre, Image Press, Cambridge, Mass). in J. ceptance angle a reflecting superposition eye. comp. 1977. nouvelle Guinot, D., Zoologie. Propositions pour une Physiol., (A) 151: 367-380. classification des Crustaces Decapodes Brachyoures, C. r. Burkenroad, M. D., 1963. The evolution of the Eucarida, hebd, Seanc. Acad. Sci., Paris, (D) 285; 1049-1052.

in relation to the fossil rec- (Crustacea, Eumalacostraca), Hafner,G. S., T. Tokarski & G. Hammond-Soltis, 1982. De-

ord. TulaneStud. 2: 1-17. Geol., velopment of the crayfish retina: A light and electron mi- Clarkson, E. N. K. & R. Levi-Setti, 1975, Trilobite and eyes croscopic study. J. Morphol., 173: 101-118. the optics of Des Cartes and Nature, 254: 663- Huygens. Hessler, R. R., 1983. A defence of the caridoid facies:

667. wherein the early evolution of the Eumalacostraca is dis-

T. 1986. and Cronin, W., Optical design evolutionary adap- cussed. Crust. Issues, 1: 145-164.

tation in J. 6: 1- crustacean compound eyes. crust. Biol,, and In: H. Kunze, P., 1979. Apposition superposition eyes. 23. Autrum of (ed.), Handbook sensory physiology: 441-502 Dahl, E,, 1963, Main lines Recent Crus- evolutionary among (Springer Verlag, Berlin). tacea. In: 11. B. Whittington & W. D. I. Rolfe (eds.), Phy- Land, M. F., 1976. Superposition images are formed by re- and evolution of 1-14 logeny Crustacea: (Mus, Comp. flection in the eyes of some oceanic decapod Crustacea. Zool,, Cambridge). Nature, 263: 764-765,

E. & T. H. Waterman, 1966. Fine structure Eguchi, patterns Land, M. F., 1981. Optical mechanisms in the higher Crusta- in crustacean rhabdoms. In: C. G. Bernhard (ed.). The cea with a comment on their evolutionary origins. In: M. functional of the 105-124 organisation compound eye: S. Laverack & D. J. Cosens Sense 31-48 (eds.), organs: Press, (Pergamon Oxford). (Blackie, London).

T. Goto & T. H. 1982. Unorthodox Eguchi, E., Waterman, M. 1984. The of Land, F., resolving power diurnal

of microvilli and intercellular in pattern junctions regular with J. superposition eyes measured an ophthalmoscope. retinular cells of the porcellanid crab Petrolisthes. Cell comp. Physiol., (A) 154: 515-533. Tiss. Res., 222: 493-513. Martin, J, W. & L. G. Abele, 1986. Phylogenetic relation-

1966. The and frontal in Elofsson, R., nauplius eye organs the ships of genus Aegla (Decapoda: Anomura: Aegli- Crustacea. and fine Morphology, ontogeny structure: 1-23 with dae), comments on anomuran phylogeny. J, crust. (Zool. Inst., Lund). Biol., 6: 576-616. Elofsson, R. & E. Dahl, 1970. The and chi- optic neuropiles Nilsson, D.-E., 1983a, Evolutionary links between apposition

asmata of Crustacea. Z. 107: 343-360. Zellforsch,, and in 302: superposition optics crustacean eyes. Nature, 1891. Exner, S., Die Physiologic der facettierten Augen von 818-821.

Krebsen und Insecten: 1-206 (Franz Deuticke, Leipzig). Nilsson, D.-E., 1983b. Refractive index gradients subserve

Downloaded from Brill.com10/11/2021 08:33:28AM via free access Contributions to Zoology, 67 (4) - 1998 235

isolation in optical a light-adapted reflecting superposi- Stevcic, Z., 1971. The main features of brachyuran evolu-

tion J. 225: 161-165. eye. exp, Zool., tion. Syst. Zool., 20: 331-340.

D.-E., 1988. A new of in Nilsson, type imaging optics com- Tiegs, O. W. & S. M. Manton, 1958. The evolution of the

332: 76-78. pound eyes. Nature, Arthropoda. Biol. Rev., 33; 255-337.

Nilsson, D.-E., 1989. Optics and evolution of the compound Tokarski, T. R. & G. S. Hafner, 1984. Regional morphologi-

In: R, C. Hardie & D, G. Facets of within the Cell Tiss. eye. Stavenga (eds.), cal variations crayfish eye. Res.,

vision: 30-73 (Springer Verlag, Berlin). 235: 387-392.

D.-E., 1990. Three Nilsson, unexpected cases of refracting Vogt, K., 1975. Zur Optik des Flusskrebsauges. Z. Natur-

in J. superposition eyes crustaceans. comp. Physiol., (A) forsch., (C) 30; 691.

167: 71-78, K., 1977. and reflection mechanisms in Vogt, Ray path cray-

Paulus, H. 1979. structure and the of the Z. F., Eye monophyly fish eyes. Naturforsch., 32: 466-468.

In: A. P. J. 1989. On the influence Arthropoda. Gupta (ed.), Arthropod phylogeny: Wagele, W., of fishes on the evolu-

299-383 Nostrand Reinhold, New (Van York). tion of benthic crustaceans. Z. zool. Syst. EvolForsch.,

Rice, A. L., 1990. The nomenclature of crabs collected dur- 27: 297-309.

ing the cruises ofHMS Porcupine in 1869 and 1870. Bull. Welsh, J. H. & F. A. Chace, 1937. Eyes of deep-sea crusta-

Br, Mus. nat. 18: 1-23. Hist., ceans. I Acanthephyridae. Biol. Bull., 72: 57-74.

Schram, F. R., 1982. The fossil record and evolution of Crus- Welsh, J. H. & F. A. Chace, 1938, Eyes of deep-sea crusta-

tacea, In: L. G. Abele (ed.), The biology of Crustacea: 93- ceans, II Sergestidae. Biol. Bull., 74: 364-375.

147 (Academic Press, New Zharkova, I, 1975. Reduction in York). S., of organs of sight deep-

M. Shelton, P. J., E. Gaten & P. J. Herring, 1992. Adapta- water Isopoda, Amphipoda and Decapoda. Zool. Zh., 54:

tions of tapeta in the eyes of mesopelagic decapod 200-208.

shrimps to match the oceanic irradiance distribution. J.

mar. Biol. Assoc. U.K., 72: 77-88, Received: 2 February 1998

Downloaded from Brill.com10/11/2021 08:33:28AM via free access