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Distinct Genetic Subdivision in Sympatric and Sibling Species of the Genus Littorina (Gastropoda: Littorinidae)

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Distinct Genetic Subdivision in Sympatric and Sibling Species of the Genus Littorina (Gastropoda: Littorinidae) Heredity 74 (1995) 1—9 Received 4 January 1994 Genetical Society of Great Britain Distinct genetic subdivision in sympatric and sibling species of the genus Littorina (Gastropoda: Littorinidae) EMILIO ROLANALVAREZ*, CARLOS ZAPATA & GONZALO ALVAREZ Departamento de Biologia Fundamental, Facultad de BiologIa, Universidad de Santiago de Compostela, 15706 Santiago, Spain Thegenetic structure of two sibling and sympatric species of the genus Littorina was compared using allozymic loci. The two species are biologically and ecologically well-known and mostly show similar life history characteristics. Three populations of L. mariae Sacchi & Rastelli and L. obtusata (L.) were studied in the Muros-Noya Ria (Galicia, NW Spain). In addition, four microgeographical subsamples taken from one of the populations were analysed for each species. Age, sex and genotypes for nine polymorphic loci were studied in 1250 snails of both species. L. mariae showed larger genetic population subdivision and lower heterozygosity levels for the loci studied than did L. obtusata. Heterozygote deficiencies were found in only a few cases in natural populations of both species, usually affecting the Lap-i locus. No significant genetic differences among age or sex classes were found. These results may be explained by the lower effective popula- tion size in L. mciriae than in L. obtusata. Known differences between these species in generation interval and population density during the winter can cause the different effective population sizes suggested. These life history characteristics appear to provide the most likely explanations for the differences in genetic differentiation and heterozygosity between the two species. A previously unknown L. mariae morph from exposed shores is tentatively suggested to be conspecific. Keywords:allozymes,flat periwinkles, genetic structure, Littorina mariae, Littorina obtusata, population subdivision. cohesiveness and the factors that promote genetic Introduction differentiation; with some factors, for example natural Theuse of allozymes as genetic markers has made selection, the influence can be in either direction (Nei, possible detailed studies of population genetic struc- 1987; Slatkin, 1987). Some authors have also ture in many animal and plant species (Ward, 1990; emphasized the factors extrinsic to the organism (biotic Lewontin, 1991). They have been used to show that and abiotic) that can influence the degree of genetic species often display different hierarchical levels of relatedness among populations (Johnson & Black, population subdivision (Johnson & Black, 1991; Wolf, 1991). It is desirable that any experiment designed to 1991), constraining or predisposing adaptive evolution find the relative importance of the different factors (Wright, 1978; Slatkin, 1987). Moreover, undetected includes some means of controlling them, at least population structure can invalidate experimental field partially. Comparative studies, among similar species hypotheses. Thus, the study of a species' genetic struc- with different genetic structures, have been used to ture is a necessary preliminary step in understanding infer the biological causes producing these differences the evolutionary potential of any taxon. (Berger, 1983; Ward, 1990). In these cases the The degree of genetic subdivision (genetic structure) uncontrolled factors are assumed to affect the in any species can be described as an equilibrium compared species in the same way. A useful group for between the evolutionary factors that promote genetic this kind of study is the North-Atlantic littorinids (Mollusca: Gastropoda), as they often have different *correspondence: Unidad de Genética, Biológicas Módulo A201, UniversidàdAutónoma de Madrid (Cantoblanco), 28049 Madrid, genetic structures and they have been well-studied Spain. biologically and ecologically. In most cases the degree 1 2 E. ROLAN-ALVAREZ ETAL. of population differentiation is related to the degree of (Rolán & Templado, 1987; Rolán-Alvarez, 1992). gene flow among populations, inferred from dispersal They show similar life history characteristics, although capabilities or breeding systems (Berger, 1983; Janson, some differences are known: L. mariae is an annual 1987a; Ward, 1990). This relationship may, however, species that feeds mainly on micro-epiphytes growing be rather inaccurate in some species (Berger, 1977). on seaweeds (Fretter & Graham, 1980; Williams, The level of population subdivision is also sensitive to 1990, 1992) whereas L. obtusata survives between 2 historical phenomena, such as bottlenecks, founder and 10 years feeding directly on seaweeds (Fretter & events (Berger, 1977; Janson, 1987b; Knight et a!., Graham, 1980; Sergievsky, 1985). In addition, L. 1987) and selection (Berger, 1983; Johannesson & mariae is usually less affected by parasites and more Johannesson, 1989). However, other relationships are affected by intertidal predators and other competing not easily found in comparative studies because of the grazers than L. obtusata, which resists more stressful difficulty in using closely related species with compar- physical conditions during low tidal periods (Fretter & able life history characteristics (Wolf, 1991). Here, the Graham, 1980; Williams, 1990,1992). population genetic structures were compared, geographically and microgeographically, in two well- known sibling species living sympatrically in the same Sampllng habitat. Tofind the geographical distribution of both species Littorinid species which have direct development more than 32 samplings were carried out in the Ria of usually present more taxonomical problems than Muros-Noya (Fig. 1). Following this, three populations species having planktonic stages (Ward, 1990). On representative of the distribution of the two species in exposed Galician shores an unusual form of Littorina the Ria were selected: ABE (Abelleira, October 1989), mariae morph has been found living on Mastocarpus AGU (Aguieira, October 1989) and PLB(Punta-Laxe- stellatus (Rolán & Templado, 1987). The transition Brava, May 1990) (Fig. 1). Around 100 adult snails between the exposed and the typical form occurred from the smallest possible area of Fucus were sampled abruptly in the area studied, suggesting a possible case in each population. This meant sampling areas of 1—2 of overlapping of valid species. In this study, these two m2 for most cases, but about 50—200 m2 in two forms were studied genetically for 10 allozymic loci to samples of L. mariae (AGU and PLB, respectively). In clarify their taxonomic status. the PLB population both species were sampled without This paper reports different genetic structures in overlapping; L. mariae was found on Mastocarpus sympatric populations of the two sibling species L. stellatus whereas L. obtusata was found on F. vesiculo- mariae and L. obtusata. The facts known of the biology sus. and ecology of these species allow suggestions to be Four microgeographical samples of both species made of the main causes of genetic differences between were taken from the Abelleira population (July 1990). them. Moreover, results of the analysis of one sample These snails were sampled over Fucus areas of about of the L. mariae exposed morph from Galicia supports 150 m2. Copulating pairs and, around them on the the suggestion that it is conspecific, perhaps an ecotype same or contiguous seaweeds, noncopulating snails of this species. were sampled in each area. This design was used in an attempt to study sexual selection in nature (Rolán- Materials and methods Alvarez et al., unpublished data). Briefly, the non- copulating snails represented more than 77 per cent of Species studied the snails from the total population in L. mariae and Littorina mariae and L. obtusata are two sibling species more than 95 per cent in L. obtusata. The noncopula- of North-Atlantic littorinids living in the Fucaceae belt ting subsamples of this later experiment were used to of intertidal zones (Fretter & Graham, 1980). Some analyse the microgeographical genetic structure of reproductive characteristics (Fretter & Graham, 1980; these species. The species were classified according to Reid, 1990) as well as some allozymic loci (Morris, shell characters in the field and this was later verified in 1979; Zaslavskaya et a!., 1992) can be used to the laboratory. distinguish the two species. They are dioecious and have direct development with crawling juveniles hatching from egg masses attached to seaweeds (Fretter & Variablesand electrophoretic methods Graham, 1980). On Galician shores both species are Sexand age classes, and genotypes for 10 allozymic found sympatrically (mainly on Fucus vesiculosus), loci, were recorded for 1250 individuals of the two although L. mariae prefers mid to lower intertidal species. Three sex classes were used: males (M), zones whereas L. obtusata prefers mid to upper ones females (F) and immature snails (I) (Fretter & Graham, GENETIC SUBDIVISION IN SIBLING SPECIES 3 Statistical analysis Variationin allelic and genotypic frequencies among samples for each locus and species were analysed using x2homogeneitytests. A pseudoprobability x2homo- geneity test was employed when low sample size within cells (less than five) was expected (Zaykin & Pudovkin, 1993). Nei's unbiased heterozygosity index (He) was used to describe allozymic polymorphism in the genetic markers studied (Nei, 1987). Two F indices were used to indicate departure from Hardy—Weinberg expectations: the Wright's F and the Robertson & Hill (1984) F' indices. The F statistic
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