A COMPARATIVE STUDY OF HYBRID ZONES IN THE POLYTYPIC LAND SNAIL ALBINARIA HIPPOLYTI (GASTROPODA PULMONATA: CLAUSILIIDAE)

by

M. SCHILTHUIZEN

(EvolutionaryBiology and SystematicZoology Section, Institute of Evolutionaryand Ecological Sciences,University of Leiden,P.O. Box 9516, NL-2300RA Leiden,The Netherlands)

SUMMARY Many species of the Mediterranean land snail genus Albinaria are highly polytypic. Because patterns of subspeciation may shed light on mechanisms of speciation in this group, three hybrid zones in A. hippolytiare analyzed. One of these, between the subspecies A. h. aphroditeand A. h. harmonia,was reported on earlier and is included as a reference. The zones were investigated by sampling across them and studying these samples conchologically, anatomically and biochemically. In general terms, the analyses show that all zones are characterised by several to many coincident clines in various types of traits. At each locality, the observed cline widths are of the same order of magnitude. In only one case was a clear association with an environmental transition observed. At all localities, some indication of recombinant disadvantage was found, in the presence of 'hybrizymes', anomalies in the reproductive system, or both. The data, viewed in the light of the snails' distribution and population structure, suggest that the hybrid zones result from secondary contact and are maintained by a balance between dispersal and selection against hybrids. This result supports a model of (sub)speciation in small, isolated populations. KEYWORDS: hybrid zones, allozymes, hybrizymes, hybrid disadvantage, natural selec- tion, conchology, anatomy, Albinariahippolyti, Clausiliidae, Crete.

INTRODUCTION

The Mediterranean pulmonate genus Albinaria has recently gained interest as a model for land snail speciation (MYLONAS et al., 1988; SCHULTES & WIESE, 1991; GITTENBERGER, 1991; KEMPERMAN, 1992; J SCHILTHUIZEN & GITTENBERGER, 1994a). The genus, which is distrib- uted in an area consisting of Greece, Cyprus, The Lebanon and parts of Turkey (NORDSIECK, 1977), is notoriously speciose: at present, 80 species are recognized (SCHILTHUIZEN, 1994, supplemented with data in NORDSIECK, 1993). Many of these species show a high degree of intraspecific differentiation and, as a consequence, are further subdi- vided into subspecies. Patterns of geographic differentiation into subspecies are often con- sidered to be of special importance to the evolutionary biologist, as they may represent an intermediate stage in a process that leads to speciation (DARWIN, 1859: 47; ENDLER, 1977; HARRISON, 1993). 262

Studies of situations where subspecies interact in hybrid zones have been particularly prominent in the recent evolutionary literature (see HARRISON, 1993, for a recent review), as the analysis of genetic contact between two differentiated populations provides a "window on the evolutionary process" (HARRISON, 1990). One of the main issues in the discussions about hybrid zones con- cerns the typc and degree of selection involved. ENDLER (1977) argued that hybrid zones may arise in situ as a direct response to varying selection pressures along an environmental gradient (exogenous selec- tion, sensu MOORE & PRICE, 1993). BARTON & HEWITT (1985) on the other hand, indicated that most hybrid zones may bc seen as the result of sccondary contact, and that they are maintained primarily by a balance between dispersal and selection against hybrids (endogenous selection, sensu MOORY & PRICE, 1993). The latter type of situation has become known as a 'tension zone' (KEY, 1968). Finally, as HEWITT (1989) and BARTON & HEWITT (1989) havc recently emphasised, exog- enous selection and endogenous selection are not mutually exclusive. Both processes may bc at work in a single hybrid zone. In Albinaria, the species A. hippolyti (Boettger) from the island of Crete is a good example of a polytypic species that is subdivided by hybrid zones. It is continuously distributed in an area about 20 X 30 km on the north-facing flank of Mt. Ida, around which are a number of smaller, isolated populations. The area is characterised by an eroded, gently undulating karst-landscape with occasional cliffs and gorges. Recently, the intraspecific taxonomy and distribution of A. hippolyti were docu- mented in detail (SCHILTHUIZEN et al., 1993). Six subspecies were recog- nised, four of which arc largely parapatric (fig. 1), namely: A. h. hippolyti (Boettger), A. h. aphrodite (Boettger), A. h. harmonia Schilthuizen et al. and A. h. holtzi Sturany (hereafter referred to with the subspecific epithets 'hippolyti', 'aphrodite', 'harmonia' and `holtzi'). The hybrid zone separating aphrodite and harmonia has recently been analyzed (SCHILTHUIZEN, 1992; SCHILTHUIZEN & LOMBAERTS, 1994b). It was found to run exactly along the cdge of a gorge, being characterised by a number of coincident clines in conchological, anatomical and biochemical traits. The clines are narrow, between 25 and 40 m wide, where the ecotonc is sharp ('edge-locality'), but wider, 80-160 m, where a valley cuts into the gorge, making the ecological transition take place over more than 1000 m ('valley-locality'). Some indirect evidence of hybrid disadvantage was found in the centrc of the hybrid zone, where aphallic individuals occur, presumably with a reduced fitness. A furthcr indication of hybrid disadvantage comes from the presence at high frequencies of a unique 'hybrizyme' (WOODRUFF, 1989) allele in the centre of the zonc. Hybrizymes probably rcsult from increased mutation rates in recombi-