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Genetic Diversity of Oceanic Island Lasaea (Mollusca: Bivalvia) Lineages Exceeds That of Continental Populations in the Northwestern Atlantic.


Abstract. Direct-developing lineages of the intertidal marine bivalve Lasaea have colonized both upstream mainland (southeastern Florida) and downstream oceanic island (Bermuda) locations in the western North Atlantic. Replicate samples from these two regional populations, separated by about 1500 km of open ocean, were sequenced for a 655-nucleotide portion of the mitochondrial (mt) cytochrome oxidase subunit I gene. Twelve haplotypes (2 Floridian and 10 Bermudan) were obtained that differed by a maximum of four substitutions among pairwise comparisons. Phylogenetic analysis yielded a parsimony network within which the mainland lineages clustered in one of the terminal branches; a mirror image of a priori expectations based on regional surface-current polarity. It is difficult, however, to envisage a plausible countercurrent dispersal mechanism. This tree topology may stem from divergent demographic processes operating on these two evolutionarily recent regional populations. The starlike phylogenetic pattern of Bermudan lineages is consistent with a history of rapid population growth. The restricted genetic repertoire and relative ecological scarcity of Floridian lineages imply either a recent founder event by unstudied Caribbean source populations or else a history of pronounced bottlenecks in population size. Bermuda's impoverished Caribbean marine biota may allow western North Atlantic Lasaea lineages to escape severe competitive interactions impacting other parts of their geographic range.


Oceanic islands have never been connected to continental landmasses and represent some of the most isolated environments on earth (Nunn, 1994). They receive their biotas solely through dispersal from geographically distant source populations and from subsequent in situ diversification (Paulay, 1994). Stretches of deep ocean surrounding such islands represent dispersal filters for benthic shallow-water marine taxa. The stringency of these filters varies according to physical parameters (e.g., distance from potential source populations, current speed and polarity) and to taxon-specific life-history traits including presence of a prolonged pelagic larval ontogeny (Scheltema, 1992; Jaeckle, 1994; Palumbi et al., 1997; Lessios et al., 1998), rafting ability (Jokiel, 1990; Helmuth et al., 1994; Ing[acute{o}]lfsson, 1995; [acute{O}] Foighil et al., 1999), and propensity for anthropogenic transfer (Carlton, 1989; Carlton and Geller, 1993; Carlton and Hodder, 1995). In general, classical oceanic island biotas exhibit a depauperate and disharmonic composition that may include relict taxa and endemic radiations (Paulay, 1994).

Bermuda is composed of a cluster of small western North Atlantic oceanic islands (32[degrees]18'N, 64[degrees]46'W) rising from a 65-[km.sup.2] carbonate platform and supported by a submerged volcanic peak (Nunn, 1994; Sterrer, 1998). It is situated within the warm Sargasso Sea section of the North Atlantic Gyre, about 1000 km east of the coast of North Carolina, and the main flow of the Gulf Stream System arcs well to the west and north of its position (Fig. 1). However, the Bermuda Platform is regularly approached by mesoscale anticyclonic eddies originating from the Gulf Stream System (Parker, 1971; Spitzer, 1989). It is generally assumed that Bermuda has remained stable throughout the Quarternary (Nunn, 1994) and, although late Pleistocene (last 130,000 years) sea-level changes ranged up to 25 m, the island group was not submerged during this period (Harmon et al., 1978, 1981).

The Bermudan shallow-water marine fauna encompasses a low level (2.4%) of endemic species and represents a moderately impoverished oceanic extension of the Caribbean fauna (Sterrer, 1986, 1998). Twenty-eight of a total of 49 common nearshore molluscs found throughout the Caribbean also occur on this oceanic island platform (Warmke and Abbott, 1961), and there is some evidence for a partial turnover of the Bermudan marine malacofauna on ecological timescales (Abbott and Jensen, 1967; Sterrer, 1986). The nearest source populations for Bermudan marine taxa of Caribbean origin are about 1500 km to the southwest, in southern Florida and the Bahamas. Based on net transport of drift bottles, this distance represents a minimum passage of 21-30 days for passive pelagic transport of larvae or rafted propagules (Jackson, 1986). Such a time frame does not pose a serious obstacle for species with long-lived pelagic larvae, but may approach the upper limit for many species with faster developing pelagic larval stages. The few data available on genetic distances of Bermudan marine invertebrates from Caribbean conspecifics are consistent with this view (Mitton et al., 1989; Hateley and Sleeter, 1993). A number of Bermudan marine faunal constituents are known to have been introduced by human agency (Sterrer, 1986, 1998), a process that is independent of current polarity or geographic distance.

The genus Lasaea is composed of minute, crevice-dwelling, intertidal clams that have a near-cosmopolitan distribution on rocky shores; its North Atlantic lineages are exclusively composed of direct-developers ([acute{O}] Foighil, 1989). Molluscan systematists generally recognize one North Atlantic species, Lasaea adansoni (Gmelin) (L. rubra Montagu; L. bermudensis Bush) (Sterrer, 1986). This systematic conclusion is based solely on shell characters and has not been corroborated by population genetic (Tyler-Walters and Crisp, 1989) and phylogenetic ([acute{O}] Foighil and Smith, 1995; [acute{O}] Foighil and Jozefowicz, 1999) studies. [acute{O}] Foighil and Jozefowicz (1999) constructed molecular phylogenetic trees for North Atlantic Lasaea lineages based on mitochondrial (mt) 16S gene variation in two continental putative source populations (Florida, the northern limit of distribution in North America; Iberia) and two oceanic island populations (Bermuda, Azores). No amphi-Atlantic genotypes were detected; Ber mudan lineages co-clustered exclusively with Floridian congeners to form a western Atlantic dade and Azorean samples formed an exclusive dade with Therian haplotypes. The western Atlantic lineages showed low levels of genetic diversity (a single Florida haplotype differed by one diagnostic nucleotide substitution from three Bermudan haplotypes), formed a shallow polytomy, and (remarkably) were sister to polyploid Australian clonal congeners in global phylogenetic trees ([acute{O}] Foighil and Jozefowicz, 1999).

Jackson (1986) attributed the presence of Caribbean species lacking an extended pelagic larval stage on Bermuda to colonization via rafting events from continental source populations. Based on present-day circulation patterns in the western North Atlantic, the hypothesis that Bermudan Lasaea populations were established by rafting events assumes that intermittent gene flow has occurred, over evolutionarily significant timeframes, from western continental margin source populations--for example, from south Florida. Island lineages are predicted to represent a subsample of mainland genetic diversity, and to contain endemic genotypes that cluster in the terminal tips of a western Atlantic dade. [acute{O}] Foighil and Jozefowicz's (1999) preliminary 16S data set had some features that were consistent with the rafting hypothesis: the three Bermudan haplotypes had close phylogenetic links to, but were genetically distinct from, the Floridian haplotype. However, these workers were unable to distinguish among ancestr al and derived relationships among the four polytomous western Atlantic mt 16S genotypes, and it was unclear how representative the sole Floridian haplotype, sampled from a single population, was of mainland regional genetic diversity.

The aim of the present study was to perform a comprehensive cladistic analysis of Bermudan and Floridian Lasaea mitochondrial lineages to test their adherence to rafting hypothesis predictions. In addition to three Bermudan populations, four populations of Lasaea were sampled along 250 km of contiguous southeastern Floridian coastline. A total of 124 specimens of western Atlantic Lasaea were sequenced for a 655-nucleotide (nt) fragment of cytochrome oxidase I, a protein-encoding mitochondrial gene that, for recently diverged lineages, typically accumulates substitutions at a faster rate than does 16S ([acute{O}] Foighil et al., 1998). Twelve western Atlantic haplotypes were obtained and yielded a phylogenetic tree topology that was a mirror image of that predicted by the rafting hypothesis.

Materials and Methods

Specimens of Lasaea were sampled in April 1998 from four southeastern Florida locations (Sebastian Inlet State Park, Brevard County; Fort Pierce Inlet State Recreation Area, St. Lucie County; Phil Foster Park, West Palm Beach; and Bill Baggs Cape Florida State Recreation Area, Key Biscayne) spanning about 250 km of contiguous coastline (see Fig. 1). The bivalves were moderately abundant in the interstices of barnacle tests at three of the sites; however, intensive sampling at the Key Biscayne site yielded only four individuals. Additional collections were taken in May 1998 from intertidal algal tufts and barnacle test interstices at three Bermudan locations (Boaz Island, the main Island at North Shore Road, and St. George's Island at the Bermuda Biological Station for Research) spanning about 20 km of the archipelago's length. At each sampling location, clams were taken from a number of microsites on the shore and pooled prior to fixation in 95% ethanol; thus a representative sample of genetic diversity from the study population was obtained.

Extensive sampling of ostensibly suitable intertidal crevice habitats elsewhere in the Caribbean by the second author (Lower Florida Keys; Dry Tortugas; New Providence, Bahamas; Puerto Rico), and by A. Frias-Martins (Jamaica), yielded no further specimens of Lasaea. Attempts to amplify the target gene fragment from a single dried museum specimen sampled from Belize (USNM# 841332) and from a small number of preserved specimens sampled from Cabo Tres Puntas, Venezuela (R.C. Bullock, University of Rhode Island, pers. comm.) were also unsuccessful. In the absence of tractable Caribbean outgroup samples, we generated homologous cytochrome oxidase subunit I (CO I) sequences from Sydney samples of Australian direct-developing polyploid Lasaea lineages ([acute{O}] Foighil and Thiriot-Qui[acute{e}]vreux, 1999) that are sister to the study populations in global phylogenetic trees ([acute{O}] Foighil and Jozefowicz, 1999; Taylor and [acute{O}] Foighil, 2000).

Twenty individuals from each of six study populations, and all four specimens from Key Biscayne, were genetically characterized by amplifying and directly sequencing a homologous 655-nt fragment of the mitochondrial CO I gene. DNA templates for thermal cycle amplification were individually extracted from entire adult Lasaea specimens using a QIAamp tissue kit (QIAGEN Inc.). The Folmer et al. (1994) CO I primer set (5'-GGTCAACAAATCATAAAGATATTGG-3'; 5'-TAAACTTCAGGGTGACCAAAAAATCA-3') was used to amplify and to sequence the target gene fragment. A negative control (no template) was included in each run of 35 cycles of amplification (1 min 94[degrees]C denaturing, 30 s 45[degrees]C annealing, 1 min 72[degrees]C extension). Double-stranded products were isolated on 1% agarose gels, excised under long-wavelength UV light, and extracted using a GeneClean (Bio 101) NaI/glass powder kit. Both strands on the target fragments were cycle-sequenced using a Big Dye DNA sequencing kit (PE Applied Biosystems), and reaction p roducts were electrophoresed on an ABI 377 automated DNA sequencer. Sequence alignments were initially performed by the CLUSTAL option of Sequence Navigator 1.0.1 (Kececioglu and Myers, 1994) and then optimized manually. Sequences were analyzed using an unweighted maximum parsimony approach (PAUP* 4.0b2a; Swofford, 1998), and root probabilities for individual haplotypes were estimated using the Castelloe and Templeton (1994) heuristic technique. Nucleotide mismatch distribution (Schneider et al., 1999) and lineage-through-time (Nee et al., 1996) analyses were respectively performed on the Bermudan lineages using Arlequin 2.0 (beta 2; Schneider et al., 1999) and the Endemic-Epidemic Phylogenetic Process Analysis (Rambaut et al., 1997).


Alignment of the 655-nt CO I fragment sequences obtained from the 124 individuals of western Atlantic Lasaea revealed 10 variable sites and 12 haplotypes (Table 1). Of the 11 nucleotide substitutions (all synonymous) detected, 8 were third codon transitions, 2 were first codon transitions, and 1 was a third codon transversion. Genetic divergence levels among the haplotypes was very low, with a maximum of four substitutions (0.6%) among pairwise comparisons. Floridian and Bermudan haplotypes exhibited one diagnostic third codon transition-i.e., no haplotype was shared among these two regional groupings. Table 2 shows the distribution pattern of the 12 haplotypes among the seven sampling sites. There was a striking discrepancy in the relative levels of haplotypic diversity and frequency in the Bermudan and Floridian samples. A total of 10 mt genotypes were contained in the combined oceanic island samples, none of which exceeded a frequency of 0.28. With the exception of a single individual from the Palm Beach population, the Floridian specimens were monomorphic for haplotype FL1.

Figure 2a shows the single most parsimonious unrooted phylogram (9 steps; 2 parsimony-informative characters; CI = 1.0; RI = 1.0) obtained by exhaustive PAUP analysis of the 10 Bermudan haplotypes. This unrooted tree had a starlike topology in which there was a distinct lack of structure; 7 of the 10 haplotypes had only a single connection. A central topological position was occupied by BDA1, the most common Bermudan genotype, which was present in all three sampled sites and was one step away from 7 of the 9 other island CO I genotypes. Heuristic estimation of outgroup weighting (Castelloe and Templeton, 1994) for each of the Bermudan mt genotypes yielded a maximum value (0.445) for BDA1 (Fig. 2a), indicating that this is probably the oldest haplotype in the Bermudan dataset.

Phylogenetic analysis of the combined Floridian/Bermudan dataset (Fig. 2b) produced a single most parsimonious tree (11 steps; three parsimony-informative characters; CI = 1.0; RI = 1.0) that maintained a starlike topology and a central position for BDA1. Floridian haplotypes were peripherally positioned in a single branch of the tree topology. BDA1 was one step removed from eight western Atlantic haplotypes, including the predominant mainland lineage (FL1), and two steps away from the remaining three lineages. In contrast, FL1 was respectively, one, two and three steps removed from two, seven, and two western Atlantic lineages. Heuristic outgroup weighting of the haplotypes in the combined tree topology (Fig. 2b) identified BDA1 (0.440) as the oldest haplotype in the western North Atlantic dataset.

Caribbean outgroup populations were unavailable to root our western North Atlantic gene tree, so we generated homologous CO I sequence for an Australian direct-developing polyploid Lasaea lineage (GenBank# AF153064) that is sister to western Atlantic congeners in global phylogenetic trees ([acute{O}] Foighil and Jozefowicz, 1999; Taylor and [acute{O}] Foighil, 2000). The Australian haplotype differed by [geq]4.4% from the western Atlantic lineages, and its utilization as an outgroup taxon produced a single most parsimonious tree (not shown; 39 steps, CI = 0.667, RI = 0.555) in which the ingroup topology (11 steps total length) was identical to that of Figure 2b and the outgroup taxon connected to BDA7, a peripheral Bermudan haplotype (Fig. 2b), by a relatively enormous branch length of 28 steps. The basal positioning of BDA7 resulted from it sharing a thymidine at position 344 with the outgroup, whereas other western Atlantic lineages had either an adenine or guanine residue (Table 1).


The COI data set corroborates [acute{O}] Foighil and Jozefowicz's (1999) preliminary mt 16S characterization of Floridian and Bermudan Lasaea populations: they are genetically very similar, yet distinct, and genetic diversity levels are higher in the oceanic island samples. Surprisingly, the parsimony network generated was a mirror image of a priori source and founder topological expectations; continental populations contained a small number of endemic genotypes that positioned peripherally in the western North Atlantic Lasaea network (Fig. 2b). Rooting of this network is necessary to test dispersal hypotheses for these two regional populations; however, rooting is complicated by the unavailability of Caribbean outgroup genotypes.

Two rooting procedures were used: phylogenetic analyses utilizing an Australian sister lineage, and calculation of relative outgroup weights for individual haplotypes based on neutral coalescence expectations. BDA7, a relatively rare Bermudan haplotype, was identified as the root of the western North Atlantic clade when an Australian sister taxon was utilized as an outgroup. This result should be viewed with caution because of the 28:1 ratio of outgroup-to-ingroup branch lengths in the analysis and because of the peripheral positioning of BDA7 in unrooted analyses (Fig. 2b). Closely related species frequently fail to accurately root intraspecific trees if intraspecific differences are much less than interspecific differences (Templeton, 1992), and coalescence theory predicts that rare haplotypes occupying cladogram tips are likely to be recently derived lineages (Donnelly and Tavar[acute{e}], 1986).

According to coalescence theory, the probability that a given haplotype is the oldest in a population is a function of its frequency and the centrality of its positioning in topological networks (Donnelly and Tavar[acute{e}], 1986; Crandall and Templeton, 1993, 1996; Beckenbach, 1994). Castelloe and Templeton's (1994) heuristic method weights interior haplotypes more heavily than tip haplotypes and differentially weights interior haplotypes by their mutational connectedness and their proximity to high-multiplicity haplotypes. It unambiguously identified BDA1, the centrally positioned (Fig. 2a) and most common Bermudan haplotype (Table 2), as the most likely candidate for the oldest Bermudan mitochondrial genotype (outgroup weight = 0.445) in our sample. BDA7 is two steps away from the central topological position (Fig. 2a), received a much, lower outgroup weighting (0.008), and cannot be accepted as the putative ancestral Bermudan lineage.

Haplotype BDA1 maintained its topological centrality and its high (0.44) outgroup weighting (Castelloe and Templeton, 1994) in combined analyses of Bermudan and Floridian lineages (Fig. 2b). Although the mainland haplotype, FL1, is by far the most common haplotype in the combined data set, its peripheral positioning in the phylogram and lack of connectedness to most of the other western North Atlantic haplotypes give it a relatively low outgroup weighting (0.297). Surprisingly, our analyses based on coalescence theory expectations indicate that the Bermudan lineage BDA1 is the oldest in our data set and represents the putative ancestral haplotype for both regional western North Atlantic populations.

Phylogenetic trees represent inferred historical relationships, and our CO I dataset, when rooted with BDA1, reveals a countercurrent topology of source (Bermuda) and founder (Florida) populations. Countercurrent gene-flow patterns have also been recently inferred for a variety of marine invertebrates (Palumbi et al., 1997; Palumbi, 1997; Benzie, 1999; Lessios et al., 1999; [acute{O}] Foighil and Jozefowicz, 1999) and may indicate that contemporary gene flow is insufficient in these cases to obscure genetic structuring produced under previous current regimes (Benzie, 1999). However, it is difficult to envisage a plausible countercurrent dispersal mechanism for the Floridian and Bermudan study populations. Although it has fluctuated in intensity, the Florida Current has apparently been a persistent feature of the North Atlantic Gyre (Keffer et al., 1988; Lynch-Stieglitz et al., 1999; Duplessy, 1999). In addition, unstudied Caribbean populations are much more plausible sources of Floridian lineages, and diagno stic genetic differences among island and mainland populations for two mitochondrial genes (COI and 165 [[acute{O}] Foighil and Jozefowicz, 1999]) rule out historical (anthropogenic) countercurrent gene flow.

It may be pertinent that the low values observed for genetic diversity are consistent with an evolutionarily recent origin for both regional Lasaea populations. The most detailed fossil-calibrated estimates of molluscan gene divergence are provided by Collins et al. (1996) for the marine snail Nucella (2%/myr/lineage for [predominantly synonymous] third codon transitional differences). The central mitochondrial genotype, BDA1, is a maximum of two nucleotide substitutions removed from all of the other members of the western Atlantic Lasaea clade. Although complicated by phylogenetic and other potential biases, application of the Collins et al. (1996) rate yields a crude maximum age estimate of 0.229 Ma for the entire western Atlantic clade and also for the Bermudan population. Intrapopulational allelic relationships are modulated by demographic history (Slatkin and Hudson, 1991; Nee et al., 1996; Lavery et al., 1996), and it is possible that the observed patterns of CO I gene variation stem from divergent dem ographic processes experienced by these two evolutionarily recent regional populations, rather than from a countercurrent pattern of gene flow.

Application of coalescence theory assumes that the study populations are at equilibrium. However, this assumption may not be met by our data set. Domination of the Floridian regional population by a single haplotype (FL1) is consistent with either a recent founder event from an unstudied source population, or else with a history of population size bottlenecking; a process that promotes stochastic elimination of novel and rare haplotypes. In contrast, the starlike allelic topology of the Bermuda samples is characteristic of a population founded by one ancestral type (presumably BDA1) that has experienced a phase of rapid growth, a process associated with lowered stochastic elimination of novel and rare lineages (Avise et al., 1984; Slatkin and Hudson, 1991). Further support for this demographic interpretation of the Bermudan population was obtained when a lineages-through-time analysis (Nee et al., 1996) (not shown) yielded profiles consistent with a historically growing population. However, nucleotide mismat ch distribution analysis of the Bermudan population using Arlequin (Schneider et al., 1999) failed to meet the sudden-expansion model (C. Cunningham, Duke University, pers. comm.), implying that the primary wave of growth for this oceanic island population may have occurred soon after the initial founding event. Differential historical rates of loss/gain of novel haplotypes in the two regional populations could act to displace ancestral haplotypes from central topological positions in the western Atlantic clade. For instance, if we were to assume that the mainland lineage FL1 represents the "true" ancestral haplotype in our western Atlantic data set, its noncentral position in the tree (Fig. 2b) might result from the repeated pruning of rare novel Floridian mt genotypes, one step removed from FL1, by sequential episodes of mainland population constrictions.

The demographic distinctions implicit in the mitochondrial genetic structure of Floridian and Bermudan Lasaea populations ultimately reflect environmental differences in the intertidal crevice habitat of this organism among the oceanic island and mainland locations. In Bermuda, Lasaea are easily sampled wherever such habitats exist ([acute{O}] Foighil, pers. observ.). In Florida, and in other Caribbean locations we investigated, Lasaea was respectively much more sporadic or nonexistent. This small clam seems to be a relatively rare component of the Caribbean rocky shore fauna. Indeed, apart from two lots from the Bahamas and a single individual from Belize, all museum records of western North Atlantic Lasaea examined in a previous survey ([acute{O}] Foighil, 1989) were from Bermuda and southern Florida.

Because of their reduced biotic diversity, oceanic islands may allow some taxa to escape competitive interactions that severely reduce survivorship in other parts of their geographic range (Paulay, 1994). Although we cannot rule out a contributing role for physical environmental factors, Bermuda may well represent such an ecological release for western Atlantic Lasaea lineages. If this interpretation is correct, future characterization of the genetic structure of Caribbean Lasaea populations, though likely to uncover novel haplotypes, is predicted to yield depauperate genetic profiles similar to that exhibited by our Floridian samples.


Our thanks to P. Mikkelsen, A. Frias-Martins, R. Bullock, and C. Simmons for facilitating our sampling efforts. The Smithsonian Institution loaned us lot USNM# 841332, and D. Graf prepared Figure 1. C. Cunningham performed the mismatch distribution analysis using Arlequin and provided pointers on inferring demographic processes from gene trees. Early drafts were critically read by M. Frohlich and A. Merriwether, and we thank C. Cunningham and two anonymous reviewers for their input. Financial support was provided by a National Geographic Research Grant, and by NSF award OCE 9617689, to D. [acute{O}] Foighil.

(*.) To whom correspondence should be addressed. E-mail:

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Publication:The Biological Bulletin
Geographic Code:1USA
Date:Jun 1, 2000
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