Table Of ContentBASTERIA, 64: 29-32, 2000
Alternative pathways in the development ofthe clausilial apparatus
in shells ofAlbinariaand Isabellaria (Gastropoda, Pulmonata,
Clausiliidae)
E. Gittenberger
InstituteofEvolutionary and EcologicalSciences & National Museum ofNatural History, c/o P.O
Box 9517, NL 2300 RA Leiden,The Netherlands
InAlbinariaandIsabellariathestep-wisedevelopmentofa G-typeinsteadofanN-typeclausilial
apparatus starts with the formation ofa lamellafulcrans instead ofa lamellaspiralis,shortly
after the initial formation ofthe lamella columellaris. The other lamellae as well asthe full-
grown clausiliumareformed later on.Itis hypothesizedthat the geneticbackgroundofsuch
an early shift in the developmentalprogramme mightbe relatively simple, facilitatingboth
parallel evolution and introgression.
Key words: Gastropoda, Clausiliidae,Albinaria, Isabellaria, clausilial apparatus, parallelism,
introgression.
INTRODUCTION
It is generally assumed that a clausilial apparatus(= CA) has originated only once in
the course ofevolution (Nordsieck, 1982), constituting an exemplary autapomorphic
character. However, after its basic structures had formed, variousadaptive refinements
ofthe CA may have evolved independently more than once. The repetitive origin of
species or subspecies with a G-type CA from N-type ancestors (Gittenberger & Schil-
thuizen, 1996; Douris et al., 1998; Gittenberger, 1998) is considered here, from both
a developmental and agenetic point ofview, onthe basis ofdatapublished by Edlauer
(1941) and personal observations on the ontogenyofboth types ofCA.
MATERIAL AND METHODS
The lamellaein both full-grown and subadult shells of G- and N-type Albinaria and
Isabellaria species were compared in order to investigate at what stage the divergence
betweenthesetwo typesbecomesapparent duringthe formationofthe CA.As complete
growth-series ofconspecific specimens were not availablefor study, the ontogenyofthe
CA had to be reconstructed on the base ofspecimens belonging to different species.
Specimens from four samples are illustrated: 1, Albinaria teres (Olivier, 1801) subsp.
[Greece, Crete, Lasithi, 7.5 km SE. ofPevkoi, 60 m alt.]; 2, id. [id., Lasithi, 6 km SSE.
ofPevkoi, 50m alt.]; 3,A. adriani(Gittenberger, 1987) [Greece, Peloponnisos, Arkadhia,
4 km SE. ofAstros atKoutroufa, 20m alt.]; 4,Isabellariasaxicola(L. Pfeiffer, 1848) subsp.
[Greece, Attiki, Imittos mts., 10 km ESE. ofAthinai]. The research materialis kept at
the National Museumof Natural History, Leiden.
30 BASTERIA, Vol. 64, No. 1-3, 2000
Figs 1-4.Theclausiliura,seen frombehind,inboth afull-grown(4)andsubadultspecimens(1-3). 1,inaddition
tothestraightclausilialstalk(s), theclausilialplate (p)beginstodifferentiate atitsend;thecolumellaris (c) and
thespiralis(sp) arealreadyprominent(Albinariateres,sample2).2,the clausiliumalreadyhasits curvature,but
theplate (p) is stillrelativelysmall; the fulcrans (f)is vaguely discernible (Isabellariasaxicola,sample4). 3, the
clausilialplateandthefulcrans (f)areprominentlypresent, but the CA isnotyet full-grown;the lower ends
ofboth thecolumellaris(c)and the subcolumellaris(sc) arebroken away (Albinariaadriani,sample3).4,thefull-
grown G-typeCA, with theplateperfectly followingthecontours ofthe aperture, includingthecurvatureof
thesubcolumellaris (sc) and thefulcrans (f) (Albinariaadriani, sample3). Scale lines 1 mm. SEM-photographs
by J.Goud(NNM, Leiden).
Gittenberger: Alternativepathways 31
Figs5-6.ThedevelopingCA,infrontalview.5,theplatehasnotyetreacheditsfinalwidthandthe columellaris
isnotyet completelyfixed tothe aperturalwall (arrows) (Albinariateres,sample 1).6, the columellarisis full-
grownbutitsoriginasaseparate additiontotheaperturalwall isstill discernible atitsbase (arrow);theinternal
crystalstructureoftheprincipalis(lp)(fig.6A)isalsoindicativeofanindependentoriginofthatlamella(Albinaria
teres, sample2). SEM-photographsbyJ. Goud(NNM, Leiden).
RESULTS AND DISCUSSION
According to Edlauer (1941), who studied the complicated CA ofHerilla bosniensis(L.
Pfeiffer, 1868) (Alopiinae), CA formationis asequential process, taking place during the
formationofthelastwhorl oftheshell (figs 1-4). Only thenthe mantleofthe snailforms
a series offolds, one after the other, betweenwhich chalkis secreted. The lamellaeare
formedafter the shell wall. They are secondarily added onto the wall, which becomes
obvious when their formationhas notyetbeencompletely finishedand a lamellais not
yetfixed over its entire length (fig. 5). The internal crystal structure ofboth a lamella
and the shell wall (fig. 6) suggests the same. CA formationstarts with the columellaris.
While this lamella is still growing, the spiralis and the clausiliumbegin to form. The
parietalis followsand thenthe subcolumellaris.With the formationoftheprincipalis and
finally the palatal folds the CA is completed.
BASTERIA, Vol. 64, M. 1-3, 2000
32
In Albinaria, as in Herilla, formationofthe spiralis and theclausilium also starts early
in development, at least in species with an N-type CA(fig. 1). In the Isabellariaspecies
and in Albinariaspecies with a G-type CA however, the growing clausilium is formed
together with the lamellafulcrans (figs 2-4), which apparently takes the place ofthe
spiralis here. Maybe the combineddevelopment ofeither the clausilialand the spiralis
mantlefold, or the clausilialand the fulcrans mantlefold, is decisive for the formation
ofafutureN-type ora G-type CA. Because of the oblique fulcrans, the clausiliummay
becomerelatively broadearly in development, beforea principalis begins to form. Later
on, there is hardly any space left for the principalis and a G-type CA is formed. The
presence ofa spiralis inearly CA development might force theequally early developing
clausiliumfurtheraway fromthepalatal wall, leaving space forthesubsequent formation
ofaprominent principalis, resulting in an N-type CA(fig. 1). Consequendy, thegenetic
background foranevolutionary shiftfromonetypeofCA toanother, maybearelatively
simple mutation, related toposition and formationofthe fulcrans, replacing thespiralis.
When co-evolutionofseveral independent CA-related morpho-genes is not required,
it is not extremely unlikely that a G-type CA will develop from an N-type in various
Albinaria species under high selection pressure, by parallel evolution or maybe even
transspecific introgression (Gittenberger, 1998). It remains to be investigated how the
two types ofCA develop in other clausiliid taxa.
REFERENCES
CHRISTELOW, A.Q., 1992. The morphologyand function ofthe clausilium ofClausilia bidentata (Strom)
(Gastropoda, Pulmonata,Clausiliidae). In: E.GITTENBERGER&J. Goud,eds, Proceedings of
the Ninth InternationalMalacologicalCongress: 107-113. Unitas Malacologica,Leiden.
DOURIS, V., R.A.D. CAMERON, G.C. RODAKIS, & R. LECANIDOU, 1998. Mitochondrial
phylogeographyofthe land snail Albinaria in Crete: long-term geologicaland short-term vicariance
effects. Evolution 52: 116-125.
EDLAUER, E., 1941. Die ontogenetischeEntwicklungdes VerschlussapparatesderClausiliiden,untersucht
an Herilla bosniensis..— Zeitschrift furwissenschaftliche Zoologie 155: 129-158.
GITTENBERGER, E., 1996. Adaptationsofthe aperture in terrestrial gastropod-pulmonateshells. —
Netherlands Journal ofZoology46: 191-205.
, 1998. Transspecific introgression in Albinaria (GastropodaPulmonata). In: R. BIELER & P.M.
MIKKELSEN, eds, Abstracts, 1998 World congress ofmalacology, Washington DC: 122. Unitas
Malacologica,Washington D.G.
—,&M.SCHILTHUIZEN, 1996.ParallelismintheoriginoftheG-type clausilialapparatus (Gastropoda,
Pulmonata,Clausiliidae). In:J.D.TAYLOR,ed.,Originandevolutionaryradiation oftheMollusca:
295-300. Oxford University Press, Oxford.
NORDSIECK, H., 1982. Die Evolution desVerschlussapparatesder Schliessmundschnecken (Gastropoda:
Clausiliidae). Archiv fur Molluskenkunde 112: 27-43.
