Geographic Variation, Niche Breadth and Genetic Differentiation at Different Geographic Scales in the Mussels Mytilus califomianus and M. edulis. J.S, Levinton ...
Marine Biology 49, 363-375 (1978)
MARINE BIOLOGY © by Springer-Verlag 1978
Geographic Variation, Niche Breadth and Genetic Differentiation at Different Geographic Scales in the Mussels Mytilus califomianus and M. edulis J.S, Levinton 1 and T.H. Suchanek 2 1Department of Ecology and Evolution, State University of New York; Stony Brook, New York, USA, and Institute of Ecology and Genetics, University of Aarhus; Aarhus C, Denmark, and 2Department of Zoology, University of Washington; Seattle, Washington, USA
Abstract
G e n e t i c d i f f e r e n t i a t i o n was i n v e s t i g a t e d in the m a r i n e m u s s e l s Mytilus californianus C o n r a d and M. edulis Linn. from the w e s t coast of N o r t h America. In a l l o p a t r y w i t h M. californianus, M. edulis occurs t h r o u g h o u t the i n t e r t i d a l zone; however, in microg e o g r a p h i c sympatry its e c o l o g i c a l range is r e s t r i c t e d to above the M. californianus m u s s e l bed and to p a t c h e s of s u b s t r a t u m o p e n e d by n a t u r a l d i s t u r b a n c e s w i t h i n the bed. Over the same g e o g r a p h i c scale, the b r o a d e r - n i c h e d M. edulis shows g r e a t e r a m o n g - l o c a l i t y g e n e t i c d i f f e r e n c e and g r e a t e r levels of p o l y m o r p h i s m than s. californianus at two enzyme loci. G e n e t i c d i f f e r e n t i a t i o n on a g e o g r a p h i c basis was inv e s t i g a t e d in M. californianus at a single rock (on a scale of meters), on an i s l a n d (on a scale of k i l o m e t e r s ) , t h r o u g h o u t a strait (on a scale of 102 k i l o m e t e r s ) , and along the west coast of N o r t h A m e r i c a (on a scale of 103 km). D i f f e r e n t i a t i o n was m i n i m a l over the w e s t coast, and could be e x p l a i n e d by m i c r o h a b i t a t differences in a local area. The m i n i m a l d i f f e r e n t i a t i o n in w e s t coast m u s s e l s relative to strong g e o g r a p h i c d i f f e r e n t i a t i o n of M. edulis on the east coast of N o r t h A m e r i c a may be r e l a t e d to the s t e e p e r l a t i t u d i n a l thermal g r a d i e n t on the east coast. Local e c o l o g i c a l l y r e l a t e d m i c r o g e o g r a p h i c v a r i a t i o n can result in b i a s e d and misl e a d i n g e s t i m a t e s of g e n e t i c h e t e r o g e n e i t y , but m i c r o g e o g r a p h i c v a r i a t i o n at enzyme loci may not be due to s e l e c t i o n at the loci i n v e s t i g a t e d or may even be due to the b r e e d i n g s t r u c t u r e of the m u s s e l p o p u l a t i o n s , as s u g g e s t e d by T r a c e y et al. (1975).
I ntroduction
The d i s t r i b u t i o n and e x t e n t of p o l y m o r p h i s m of a l l o z y m i c g e n e t i c v a r i a t i o n has b e e n s t u d i e d i n t e n s i v e l y over the last decade as the r e s u l t of p i o n e e r i n g studies d e m o n s t r a t i n g u n e x p e c t e d l y large levels of genic p o l y m o r p h i s m in n a t u r a l p o p u l a t i o n s (see Lewontin, 1974). Although new kinds of v a r i a b i l i t y are cont i n u o u s l y being discovered, g e n e r a l exp l a n a t i o n s for the m a i n t e n a n c e of this v a r i a t i o n still elude us. A l t h o u g h dist r i b u t i o n s of gene and g e n o t y p i c frequencies c o n s i s t e n t w i t h natural s e l e c t i o n have been r e p o r t e d in m a r i n e species (Johnson, 1971; S c h o p f and Gooch, 1971a; Koehn et al., 1973, 1976; Levinton, 1973; M i t t o n et al., 1973; L e v i n t o n and Fundillet, 1975; Wilkins, 1975), a m a j o r pred i c t i o n of the s e l e c t i o n h y p o t h e s i s is not v i n d i c a t e d by the data. The e x p e c t e d r e d u c t i o n of g e n e t i c v a r i a b i l i t y in the deep sea has not b e e n o b s e r v e d (Schopf
and Gooch, 1971b; Somero and Soule, 1974; V a l e n t i n e and Ayala, 1975). A l t h o u g h L e v i n t o n (1973) found a c o r r e l a t i o n between h e t e r o z y g o s i t y and e n v i r o n m e n t a l h e t e r o g e n e i t y at an LAP and a GPI enzyme locus in 6 m a r i n e b i v a l v e species, a later a m o n g - s p e c i e s study (Levinton, 1975) showed this c o r r e l a t i o n at only the GPI locus. Mathers' (1975) and Wilkins' (1975) data on GPI v a r i a t i o n in b i v a l v e s of Irish w a t e r s have c o n f i r m e d this observation. Studies of g e o g r a p h i c and m i c r o g e o g r a p h i c v a r i a t i o n in m a r i n e species have p r o v e n fruitful in u n d e r s t a n d i n g the potential s e l e c t i v e s i g n i f i c a n c e of allozymic v a r i a t i o n in m a r i n e species. Williams et al. (1973) s h o w e d that latituder e l a t e d g e n e t i c d i f f e r e n t i a t i o n into smooth clines occurs w i t h i n one generation among p o p u l a t i o n s of newly a r r i v e d juvenile A m e r i c a n eels (Anguilla rostrata), p r e s u m a b l y d e r i v e d from the same panm i c t i c gene pool. Further, a m o n g - l o c u s
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J.S. Levinton and T.H. Suchanek: Genetic Differentiation in Mussels
differences in clinal variation have been found for marine species along coasts (Williams et al., 1973; Christiansen and Frydenberg, 1974; Koehn et al., 1976). For example, C h r i s t i a n s e n and Frydenberg (1974) found that two unlinked loci of the eel pout zoarces v i ~ parus show parallel clines in Danish waters, whereas two other unlinked allozyme loci m a i n t a i n constant gene frequencies over this same geographic range, They argue convincingly that concurrent clinal and constant v a r i a t i o n cannot be reconciled w i t h an hypothesis employing random genetic drift. Smooth clinal variation, although commonly observed (O'Gower and Nicol, 1968; Johnson, 1971; Schopf and Gooch, 1971a; Johnson and Utter, 1973; Koehn et al., 1976; and others), is consistent with models of isolation and recent p o p u l a t i o n mixing, as well as selection (Endler, 1973). M i c r o g e o g r a p h i c variation, correlated with environmental variables, has been commonly reported as evidence for the selective maintenance of enzyme polymorphisms. Allele and genotypic frequencies may vary regularly with intertidal height (Balegot, 1971; Koehn et al., 1973; Levinton and Fundiller, 1975). Genetic differences between juveniles and adults in the same m i c r o h a b i t a t may indicate natural selection (Koehn et al., 1973; Mitton et al., 1973; Levinton and Koehn, 1976). As in m a c r o g e o g r a p h i c variation, among-locus differences are found in microgeographic variation (Balegot, 1971; Levinton and Fundiller, 1975; Levinton, unpublished data). Unfortunately, microgeographic variation that fails to correlate with anything is probably not reported in the literature. The mode of reproduction of marine invertebrates has also been implicated in explanations of gene-frequency v a r i a t i o n over space. Due to p r e s u m e d extensive gene flow, marine species with longlived p l a n k t o t r o p h i c larvae should have less m a c r o g e o g r a p h i c genetic differentiation than brooders. Such a general cotrelation has been found among species of Littorina (Berger, 1973) and in a comparison of the brooding periwinkle Littorina saxatilis and the pelagic disperser Nassarius obsoletus (Snyder and Gooch, 1973). There is, however, an ecological difference confounded with these results. Brooding snails tend to occur in the high intertidal zone, where interlocality differences can be pronounced. Vermeij (1972) suggests that the trend for brooding and crawl-away larval dispersal to occur in high intertidal habitats is because of habitat patchiness. Limited dispersal may allow populations to genetically adapt to local environments in
the absence of extensive gene flow that can dilute such local differentiation. Thus, the greater d i f f e r e n t i a t i o n observed in brooders might be due to strong and locally varying selective pressure, acting in concert with the restriction of gene flow with neighboring populations. We here report on several surveys of genetic differentiation in mussel populations of Mgtilus californianus Conrad and M. edulis Linn. on the west coast of North America. These surveys are designed to reveal the relative roles of m i g r a t i o n and selection in the geographic distribution of allele frequencies. We have examined the extent of differentiation at two enzyme loci in the mussel M. californianus on a single rock (scale of meters), an island (scale of kilometers), a strait (scale of 102 kilometers), and along the west coast of North America (scale of 103 kilometers). If isolation is an important factor in determining gene frequencies, then differentiation should increase with geographic scale. L e v i n t o n and Fundiller (1975) demonstrated that variation in a leucine aminopeptidase locus in M. californianus on an island was correlated with intertidal height. Tracey et al. (1975) observed no m i c r o g e o g r a p h i c structure, and employed a model of breeding structure and selection to explain patterns of heterozygote deficiencies in M. californianus similar to those reported by Levinton and Koehn (1976). We have taken a different approach in investigating the role of m i g r a t i o n versus selection. Rather than comparing species of differing reproductive and dispersal modes, we have compared species w i t h similar p l a n k t o t r o p h i c larval dispersal, but differing ecology. Genetic d i f f e r e n t i a t i o n at two loci was compared among localities in the Strait of Juan de Fuca, W a s h i n g t o n State, USA, for the California mussel Mytilus californianus and the bay mussel M. edulis. M. californianus is a large mussel, adapted to open coasts of high wave energy. It has a thick byssus, robust shell, occurs in open marine waters, and is absent from locales of estuarine salinity (see Harger, 1968, 1970, 1972; Paine, 1974). By contrast, M. edulis is smaller and occurs in w a v e - e x p o s e d outer coast, strait, and estuarine localities. M. edulis occurs in the upper intertidal in large numbers at Tatoosh Island near Cape Flattery, Washington. This island has a w a v e - e x p o s e d coast, and is mainly dominated by M. californianus. M. edulis further occurs in broad sympatry with M. californianus along exposed localities of open marine salinity in the Strait of Juan de Fuca, Wash-
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ington, USA. In such l o c a l i t i e s (e.g. a single rock, n o r t h of False Bay, San I c e b e r g P o i n t of Lopez I s l a n d - L o c a l i t y J u a n Island, W a s h i n g t o n (Locality FB). IP in Fig. 2) M. e d u l i s o c c u r s in the U s i n g an a l i d a d e and p l a n e table, relah i g h i n t e r t i d a l , above the zone of M. ca- tive i n t e r t i d a l h e i g h t s w e r e d e t e r m i n e d l i f o r n i a n u s . This is also true on the to be w i t h i n a v e r t i c a l range of 50 cm. o u t e r c o a s t l o c a l i t i e s of T a t o o s h I s l a n d Finally, a set of samples of b o t h M. ca(TA, Fig. I) and La Push (LP, Fig. I). M. l i f o r n i a n u s and M. edulis w e r e taken along edulis also c o l o n i z e s , t h r o u g h larval set- the W a s h i n g t o n coast of the S t r a i t of tlement, p a t c h e s w i t h i n the M. c a l i f o r n i a Juan de Fuca and the San Juan Islands nus b e d that have b e e n s t r i p p e d of M. ca(Fig. 2). W h e r e p o s s i b l e both species l i f o r n i a n u s due to s t o r m damage (Suchanek, w e r e t a k e n from the same location. Some u n p u b l i s h e d data). Finally, S. edulis ocl o c a l i t i e s h a d only one species (Table curs t h r o u g h o u t the i n t e r t i d a l zone in I), and we u n f o r t u n a t e l y d i s c o v e r e d M. bays and near rivers of low salinity. On w a v e - e x p o s e d rocks n o r t h of the m o u t h of the C o l u m b i a R i v e r estuary, USA, M. edulis o c c u r s w h e r e M. c a l i f o r n i a n u s w o u l d p r o b a b l y occur, w e r e the s a l i n i t y not estuarine. Thus, M y t i l u s e d u l i s o c c u p i e s a b r o a d e r J7C range of h a b i t a t s than M. californianus. 5O' T h e i r d i s p e r s a l mode is similar. Both have p e l a g i c larvae of s e v e r a l w e e k s dur a t i o n (see Seed, 1976). However, on the outer Washington coast larval settlement t6C of M. c a l i f o r n i a n u s is sparse and continuous t h r o u g h o u t the year, w h e r e a s that of M. edulis is m o r e t e m p o r a l l y discrete, w i t h a large w i n t e r peak (Suchanek, un4C p u b l i s h e d data). D i f f e r e n c e s in g e o g r a p h ic d i f f e r e n t i a t i o n , t h e r e f o r e , m a y be re15(; lated to the d i f f e r e n t levels of e c o l o g i cal s p e c i a l i z a t i o n b e t w e e n the species. We have also s u r v e y e d genic h e t e r o z y g o s i ty in s e v e r a l e n z y m e loci for a s i m i l a r interspecific comparison.
SO'
Materials and Methods
S a m p l e s of M y t i l u s c a l i f o r n i a n u s and M. edulis w e r e c o l l e c t e d from the i n t e r t i d a l zone a l o n g the w e s t c o a s t of N o r t h A m e r ica and w i t h i n the S t r a i t s of J u a n de F u c a and San J u a n I s l a n d s r e g i o n in W a s h i n g t o n (Table I). All samples of M. c a l i f o r n i a n u s taken from the w e s t C o a s t (Fig. I) w e r e c o l l e c t e d as close as poss i b l e to the m i d p o i n t of the i n t e r t i d a l v e r t i c a l range of the m u s s e l bed. Further, s a m p l e s of j u v e n i l e (O+ year class -- here d e f i n e d as i n d i v i d u a l s
