Most models of sympatric speciation have assumed strong disruptive natural selection leading to genetically based ecological diversification (Tauber & Tauber, 1989). Following the biological species concept of Mayr (1942), the two diverging populations will become different species when there is complete reproductive isolation between them. Isolation may evolve as a correlated response to the different action of natural selection on each population, or may be the result of selection acting through a process of reinforcement (Dobzhansky, 1940). The latter can be defined as the evolution of prezygotic isolating barriers in zones of overlap or hybridization as a response to selection against hybridization (Howard, 1993). Therefore, natural selection may be indirectly or directly involved in both steps of sympatric speciation: the establishment of a stable polymorphism and the evolution of reproductive isolation.
Hybrid zones are invaluable natural laboratories in which to study the role of natural selection in sympatric speciation (Hewitt, 1988; Barton & Hewitt, 1989; Harrison, 1993; Arnold, 1997). They are defined as places where two or more population of individuals, distinguishable on the basis of one or more heritable characters, overlap spatially and temporally, and cross to form viable and at least partially fertile offspring (Arnold, 1997). Studies of natural selection in hybrid zones have traditionally been based on estimates of viability or fecundity (see Arnold, 1997 for a review of hybrid zones), and sexual selection has received only limited attention (Butlin, 1989; Parsons et al., 1993). However, sexual selection is also a potentially strong mechanism contributing to the maintenance of hybrid zones and to the possible evolution of reproductive isolation (Endler, 1986; Vamosi & Schluter, 1999). Sexual selection can amplify spatial patterns of variation in male traits (Lande, 1982) and can lead to reproductive isolation, either by favouring assortative mating in a Fisher runaway-type process (Lande, 1981; Turner & Burrows, 1995; Payne & Krakauer, 1997) or acting against the adult hybrids (Vamosi & Schluter, 1999), or both. Most studies of the role of sexual selection in sympatric speciation have involved laboratory studies or theoretical analysis of models, and few estimates of sexual fitness have been obtained in the field, where the evolutionary consequences of the results are clearer (Vamosi & Schluter, 1999).
The organism and the problem
Littorina saxatilis (Olivi) is an intertidal snail that shows an extensive habitat-associated morphological variation (Reid, 1996), in some cases even at a microgeographical scale (Janson, 1983; Johannesson et al., 1993; Johannesson & Johannesson, 1996). It has direct development, separate sexes and internal fertilization, and mating pairs can be found all year round (Johannesson et al., 1995). The male climbs his partner’s shell in a counter-clockwise manner before inserting his penis into the mantle cavity of his partner (Saur, 1990).
Populations of L. saxatilis on the Galician coast (NW Spain) provide an extreme example of within-shore dimorphism in the shell, anatomical and behavioural characters (Johannesson et al., 1993; Rolán-Álvarez et al., 1996, 1997). There are two very different morphs, associated with different shore levels. The smooth and unbanded (SU) morph has a small body size and inhabits the lower, more wave-exposed shore, dominated by mussels (Mytilus galloprovincialis); the ridged and banded (RB) morph is larger and inhabits the upper, more sun-exposed shore, dominated by barnacles (Chthamalus stellatus) (Johannesson et al., 1993).
In the midshore, which is covered by a mixture of mussel and barnacle patches, the two pure morphs live and reproduce sympatrically, remaining phenotypically distinct even when they occur together under the same environmental conditions. There is much additional evidence for genetic differences between the pure morphs: they ‘breed true’ in the laboratory (Johannesson et al., 1993), there is a partial genetic barrier between them, revealed by allozymic polymorphisms (Rolán-Álvarez et al., 1996), and there is also a clear genetic basis for traits that differentiate between the two morphs, such as growth rate (Johannesson et al., 1997) as well as several quantitative shell traits (Carballo et al., 2001). The pure morphs hybridize in the midshore (Rolán-Álvarez et al., 1997) where both heteromorphic mating pairs and snails with intermediate phenotypes are found in varying frequencies. However, despite the finding of heteromorphic matings, the two pure morphs mate assortatively in the midshore (Johannesson et al., 1995; Rolán-Alvarez et al., 1999), partially because of the nonrandom microdistribution over the mussel and barnacle patches, and partially because of differences in behavioural discrimination (Johannesson et al., 1995; Otero-Schmitt et al., 1997; Rolán-Alvarez et al., 1999). In spite of the distribution of morphs along the shore gradients, it is possible to observe clinal variation for many traits, even within morphs.
This hybrid zone is likely of primary origin, as, although changes in allozyme frequency show that there is some genetic isolation between the morphs on a microgeographic scale, there is no evidence of correlation between morphological and genetic differences on a broader scale, as expected if different populations from the same morph shared a common allopatric origin (Johannesson et al., 1993). Thus, the polymorphism in the Galician population of L. saxatilis probably evolved by strong differential selection between upper and lower shore. In fact, different components of natural selection have already been studied, namely: viability (Rolán-Álvarez et al., 1997), fecundity (Cruz et al., 1998), male fertility (Johannesson et al., 2000) and sexual selection (Johannesson et al., 1995; Rolán-Álvarez et al., 1995, 1999). These studies have shown that the polymorphism seems to be maintained by natural selection, as one morph has the highest viability in the upper shore and the other in the lower shore (Rolán-Álvarez et al., 1997). The role of the other fitness components in the distribution of morphs was not as clear and, in general, hybrids were not inferior. All of these studies involved comparisons between average values of morph traits and until now, none of the selection components has been studied in relation to the continuous phenotypic variation that exists between and within morphs, which is required to understand how selection models the observed clinal variability.
In this study, we have investigated the possible role of sexual selection in the maintenance of the polymorphism and in the evolution of reproductive isolation in the hybrid zone. The existence of such a role would be indicated by the inferiority of hybrids or divergent sexual selection acting on some phenotypic trait that separates the pure morphs. To study the strength and form of natural selection and to identify the traits on which it is acting, we carried out multiple regressions of an estimate of sexual selection (probability of mating) on phenotypic traits (Lande & Arnold, 1983).