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Genetic Evidence for the Cryptic Species Pair, Lottia Digitalis and Lottia Austrodigitalis and Microhabitat Partitioning in Sympatry

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Genetic Evidence for the Cryptic Species Pair, Lottia Digitalis and Lottia Austrodigitalis and Microhabitat Partitioning in Sympatry Mar Biol (2007) 152:1–13 DOI 10.1007/s00227-007-0621-4 RESEARCH ARTICLE Genetic evidence for the cryptic species pair, Lottia digitalis and Lottia austrodigitalis and microhabitat partitioning in sympatry Lisa T. Crummett · Douglas J. Eernisse Received: 8 June 2005 / Accepted: 3 January 2007 / Published online: 14 April 2007 © Springer-Verlag 2007 Abstract It has been proposed that the common West rey Peninsula, CA to near Pigeon Point, CA, where L. digi- Coast limpet, Lottia digitalis, is actually the northern coun- talis previously dominated. terpart of a cryptic species duo including, Lottia austrodigi- talis. Allele frequency diVerences between southern and northern populations at two polymorphic enzyme loci pro- Introduction vided the basis for this claim. Due to lack of further evi- dence, L. austrodigitalis is still largely unrecognized in the Sibling species are deWned as sister species that are impos- literature. Seven additional enzyme loci were examined sible or extremely diYcult to distinguish based on morpho- from populations in proposed zones of allopatry and symp- logical characters alone (Mayr and Ashlock 1991). Marine atry to determine the existence of L. austrodigitalis as a sibling species are ubiquitous, found from the poles to the sibling species to L. digitalis. SigniWcant allele frequency tropics, in most known habitats, and at depths ranging from diVerences were found at Wve enzyme loci between popula- intertidal to abyssal (Knowlton 1993). We will refer to spe- tions in Laguna Beach, southern California, and Bodega cies that are indistinguishable morphologically, whether or Bay, northern California; strongly supporting the existence not they are sister species, as “cryptic species” and will of separate species. Both species exhibit two microhabitat restrict our use of “sibling species” to cryptic species for morphotypes, a gooseneck barnacle morph in the mid-inter- which there is phylogenetic evidence for sister species tidal zone and a rock morph in the high-intertidal zone. In status. Cryptic species that are not sibling species could sympatry, L. austrodigitalis was more abundant higher in exhibit similar characteristics due to either convergence the intertidal on rocks, whereas L. digitalis was more abun- or the retention of more ancient plesiomorphic similarity. dant lower in the intertidal on barnacles. This Wnding sup- Although this deWnition of sibling species is somewhat ports earlier claims of microhabitat partitioning in this more restrictive than “Modern Synthesis” vintage and more sibling species pair. In addition to this Wnding, the transi- recent deWnitions (Mayr and Ashlock 1991; Knowlton tion zone between the species was found to have shifted 1993), we believe that it is helpful for distinguishing substantially northward in only two decades, from Monte- between alternative situations where there might or might not be phylogenetic estimates available. Cryptic species are often overlooked in the marine environment as a result of Communicated by P.W. Sammarco. several factors: (1) the diYculty of discovering reproduc- tive isolation when it occurs, (2) scarcity of well preserved L. T. Crummett · D. J. Eernisse soft tissues in museum collections, (3) the confounding fac- Department of Biological Science, California State University, tor of normal intraspeciWc geographic variation, and (4) the Fullerton, CA 92834-6850, USA assumed potential for long-distance dispersal along coast- lines being equated with expectations for broad geographic & L. T. Crummett ( ) ranges (Knowlton 1993). Sibling species are common Department of Zoology, University of Florida, Gainesville, FL 32611-8525, USA in various marine taxa such as poriferans (Sole-Cava e-mail: [email protected] and Thorpe 1986; Boury-Esnault et al. 1992), cnidarians 123 2 Mar Biol (2007) 152:1–13 (McCommas and Lester 1980; Bucklin and Hedgecock tian Islands, Alaska to Baja California Sur, Mexico 1982; Buss and Yund 1989), mollusks (Mastro et al. 1982; (McLean 1978; Morris et al. 1980; Lindberg 1981; Lind- Moyse et al. 1982; Ward and Janson 1985; Chaney 1987), berg et al. 1987; Shanks 1998; Holyoak 1999). Limpets crustaceans (Mathews et al. 2002; Strasser 2003; Asakura identiWed as L. digitalis from Santa Cruz, California, were and Watanabe 2005; MacPherson and Machordom 2005) shown to be morphologically plastic (Lindberg and Pearse and echinoderms (Manwell and Baker 1963; Lessios 1981; 1990) exhibiting a lower-proWle broad morphotype with Nishida and Lucas 1988; Matsuoka and Hatanaka 1991). mottled brown, black, green, or golden coloration when it Estimates of marine biodiversity are increasing as more inhabits vertical rock faces and a taller and narrower mor- sibling species are being discovered. For example, the photype that is white with black stripes when it dwells on copepod genus Tisbe has grown from a few to over 63 spe- gooseneck barnacles (Pollicipes polymerus). These “rock” cies (Marcotte 1984) as a result of discovering signiWcant and “barnacle” morphotypes are superbly camouXaged to allozyme diVerences. Further, eight sibling species of poly- match their respective habitats. Murphy (1978) proposed chaetes were identiWed within what was formerly a single that L. digitalis ranged mostly from the Aleutian Islands, species, Capitella capitata, based on diVerences in chromo- Alaska to Point Conception, California, becoming consid- some number (Grassle et al. 1987). Analysis of mitochon- erably rarer to the south into southern California. In con- drial gene regions for limpets that at one time had all been trast, L. austrodigitalis ranged continuously from the referred to as Lottia strigatella (Carpenter 1864) conWrmed northern PaciWc coast portions of Baja California Sur, Mex- the validity of the more northern L. paradigitalis (Fritch- ico to Point Conception, California, including a more north- man 1960) and also revealed previously unrecognized spe- ern population on Monterey Peninsula in Central California cies in the south (Simison and Lindberg 2003). (Murphy 1978). Valentine (1966) observed that Monterey The scientiWc evidence for establishing a cryptic species Bay is 2–3°C warmer than the waters to the north and south complex can be somewhat controversial, like that of the and that some warmer-water organisms are found there. limpet pair, Lottia digitalis (Rathke 1833) and L. austrodig- After comparing limpets from 10 locations (Fig. 1) italis (Murphy 1978). L. digitalis is a common temperate between Corona Del Mar, CA (33.59°N) and Yachats State northeastern PaciWc limpet species that occupies a broad Park, Oregon (44.30°N), Murphy (1978) reported allozyme band within the rocky intertidal habitat, from the mid to diVerences attributed to the diVering distributions of L. dig- high tide zone, and has conventionally been thought to italis versus L. austrodigitalis. The rock and barnacle exhibit a large geographic range spanning from the Aleu- microhabitats at each site were sampled equally. Murphy Fig. 1 A map of the California coastline showing the location of collection sites from the current study as well as those from Murphy’s studies (1978, 1983). Current collection sites are underlined while Murphy’s col- lection sites are marked with an asterisk. Those sites sampled in both studies are underlined and marked with an asterisk. From south to north: Laguna Beach (LAG), Point Mugu (MUG), Gaviota Beach (GAV), Cayucos (CAY), San Simeon (SSM), Mill Creek (MIL), Monterey Penin- sula (MON), Santa Cruz (SCZ), Pigeon Point (PPT), and Bodega Bay (BOD) 123 Mar Biol (2007) 152:1–13 3 reported statistically signiWcant diVerences in allele fre- using horizontal starch gel electrophoresis, a well-estab- quencies at the leucine amino peptidase (LAP, EC 3.4.11.1) lished technique that has been used extensively in the exam- and glucose phosphate isomerase (GPI as “PGI”, EC ination of cryptic species (Ward and Janson 1985; Staub 5.3.1.9) loci between the three northernmost populations et al. 1990; Matsuoka and Hatanaka 1991; Crawford et al. (Yachats, OR; Bodega Head, CA; Santa Cruz, CA) and the 1996; Manchenko and Kulikova 1996) as well as in taxo- two southernmost populations (Point Mugu, CA and nomic studies (Ayala 1983; Bullini 1983; Thorpe 1983). By Corona Del Mar, CA). Further, he reported that the LAP sampling more allozyme loci, we generated additional locus could be used by itself as a diagnostic species marker data supporting the hypothesis that L. austrodigitalis and with 98.8% probability of assigning an individual to the L. digitalis are distinct species and attempted to characterize correct species. No evidence for hybridization was found in current species boundaries. We also investigated multiple the zone of sympatry, which spanned from Gaviota State sympatric populations for evidence of ecological partition- Beach, CA to Santa Cruz, CA (Fig. 1). Judging from the ing between rock and barnacle microhabitats. fact that Murphy’s proposal has been largely ignored, these earlier Wndings were not enough to convince limpet taxono- mists and biologists working on these limpets that L. digi- Materials and methods talis was actually the northern counterpart of a sibling (or cryptic) species duo (Abbott and Haderlie 1980; Ricketts Collection of samples et al. 1985; Lindberg et al. 1987, 1998; Hahn and Denny 1989b; Lindberg and Pearse 1990; Hobday 1995; Denny Limpet populations were sampled from six Californian and Blanchette 2000; Denny 2000). Only one gene locus intertidal sites (Table 1; Fig. 1). Collections were made showed strong
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