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BULLETIN OF MARINE SCIENCE, 39(2): 550-564, 1986 LARVAL INVERTEBRATE WORKSHOP IS GENE FLOW FROM PELAGIC LARVAL DISPERSAL IMPORTANT IN THE ADAPTATION AND EVOLUTION OF MARINE INVERTEBRATES? Dennis Hedgecock ABSTRACT Pelagic larvae provide a potent means of dispersal among conspecific populations of marine organisms. Whether the gene flow resulting from this dispersal confers a short-term, adaptive advantage by damping genetic responses of local populations to ephemeral conditions, and whether this translates into a long-term, evolutionary stability of genetic cohesiveness among widespread populations, however, are open questions. Differentiation of local, con specific populations, despite larval dispersal, appears to be the rule rather than the exception for such organisms. Geographic patterns of electrophoretically detectable allozyme variation in the lobster Homarus and the barnacle Balanus glandula provide examples of genetic divergence on both macro- and microgeographic scales. For the lobster, differentiation of Gulf of St. Lawrence and Atlantic populations with respect to allozyme and reproductive physiOlogical traits may be due to a previously unsuspected barrier to successful larval production on the Scotian shelf. For the barnacle, significant microgeographic genetic heterogeneity is found despite a qualitative homogeneity over broad regions as expected from larval dispersal; selection after settlement rather than heterogeneity of recruits appears to explain local divergence in the face of substantial gene flow. Thus, differentiation of populations of marine invertebrates having pelagic larvae can arise from either physical or biological barriers to larval dispersal or from differential survival or fecundity of immigrants. Where diversifying selection follows coarse-grained patterns of environmental heterogeneity, gene flow by larval dispersal would appear to be maladaptive. If the adaptive significance of the pelagic larva lies not in the benefits of gene flow, it may reside instead in the benefits of migrating to nursery habitats. Long-term, evolutionary consequences are more difficult to evaluate. The hypothesis that distributions of planktotrophic versus lecithotrophic fossil molluscs differ because of high gene flow in the former and low gene flow in the latter is not supported by neontological population genetic evidence. Also, the widespread existence of cryptic sibling species cautions against relying upon estimates of speciation and extinction rates for fossil taxa that are morphologically defined. Gene flow is genetically effective migration, an exchange among conspecific populations of successfully fertilizing gametes or of individuals who survive to reproduce in the population to which they migrate. Gene flow depends not only on the rate of exchange of migrants, but perhaps more importantly upon migrant fitness, which in tum depends on spatial and temporal variability of the environment. Gene flow is an adaptive feature, if it "permits populations to respond under natural selection to long-term, widespread fluctuations in the environment while damping the response to local, ephemeral oscillations" (Levins, 1964). Finally, gene flow is said to preserve the cohesiveness and integrity of biological species (Mayr, 1963). The pelagic larvae of many marine invertebrates clearly disperse. But do they provide high rates of gene flow resulting in genetic cohesion among geographically separated populations? Is larval dispersal thereby adaptive in buffering against spatial and temporal variability of adult habitats? Do species with pelagic larvae live longer in evolutionary time? Most authors who have considered the genetic and evolutionary consequences of larval dispersal (Scheltema, 1971; 1975; 1978; Gooch, 1975; Crisp, 1978; sso HEDGECOCK: PELAGIC LARVAL DISPERSAL AND GENE FLOW 551 Burton, 1983) have acknowledged the balance, first described by Wright (1931), that shifts between the forces of gene flow-which tends to make gene frequencies uniform among populations-and of genetic drift and natural selection-which act to diversify populations. The tendency among marine biologists, however, has been to equate potential for larval dispersal with high rates of gene flow, to see the balance of evolutionary forces tipped towards genetic cohesion among benthic adult populations, perhaps even to view the pelagic larva as an adaptation for gene flow. Theory (Levins, 1964; Strathmann, 1982) and empirical observations (Burton, 1983) demonstrate quite the opposite, however, leading to the viewpoint that the population genetic role of pelagic larvae has been overestimated, their adaptive significance perhaps misinterpreted. A similar opposition to Mayr's (1963) regard for the importance of gene flow among terrestrial organisms was expressed by Ehrlich and Raven (1969). The first question in determining the effectiveness of pelagic larvae as agents of gene flow, is whether potential for larval dispersal, as judged by factors such as the duration of the planktonic phase and the strengths of prevailing oceanic currents, is realized as successful migration of individuals. The next question is whether dispersing larvae successfully survive and reproduce. Finally, we ask whether actual levels of gene flow among populations of marine invertebrates with pelagic larvae enhance population mean fitness and promote evolutionary durability. Our ability to measure the rate and effectiveness of gene flow in natural populations is methodologically severely constrained. No effective means of conducting mark-release-recapture studies on marine invertebrate larvae has yet been devised. Techniques such as gel electrophoresis may seem promising for measuring gene flow, but instantaneous or static observations of gene frequencies reflect several, usually unknown, population genetic parameters-effective population sizes, selection coefficients, mutation rates, migration rates-and are made in ignorance of whether populations are in equilibrium (Hedgecock, 1982). Slatkin (1981) suggests that the average frequency of alleles computed for different numbers of samples in which those alleles are detected can be used to distinguish among high, intermediate and low levels of gene flow in natural populations. His analysis of data sets available from the literature shows the mussel Mytilus edulis and the milkfish Chanos chanos, for example, to have high levels of gene flow since alleles at appreciable frequencies are widely shared by populations. Even if we are reasonably certain that gene flow is high for species with pelagic larvae, the important question to address is whether high gene flow retards local adaptive differentiation of benthic adult populations. Among terrestrial organisms genetic differentiation and even reproductive isolation of populations in the face of high gene flow have been demonstrated (Koopman, 1950; Thoday and Gibson, 1962; McNeilly and Antonovics, 1968; Ehrlich and Raven, 1969; Antonovics and Bradshaw, 1970). For marine invertebrates, there is now substantial evidence for local adaptive divergence despite high gene flow (Burton, 1983), and there may be cause for careful investigations of incipient reproductive isolation in some cases. Differentiation of con specific populations has been shown in two studies that have been made in my laboratory, one on the lobster Homarus americanus and the other on the barnacle Balanus glandula. The study of lobster allozyme variation was completed 10 years ago, but recent information both on geographic variation in the photoperiodic response of reproductive females and on larval recruitment to the Atlantic coast of Nova Scotia sheds new light on interpretation of the allozyme data. Results from a survey of allozyme variation in B. glandula 552 BULLETIN OF MARINE SCIENCE. VOL. 39, NO.2. 1986 led me previously to propose that genetic variation on a microgeographic scale might be caused not by selection after settlement but by variation in the genetic composition of successful recruits (Hedgecock et aI., 1982; Hedgecock, 1982). This hypothesis, however, has conclusively flunked its first test in Balanus, leaving selection as the most likely explanation of geographic variation in this barnacle. These cases, described in detail below, together with examples from the literature, support the viewpoint that, for many marine invertebrates, pelagic larval dispersal does not provide adaptive and evolutionarily significant gene flow. SUBDIVISION OF THE AMERICAN LoBSTER POPULATION Homarus americanus is distributed from North Carolina to Newfoundland and has a pelagic larval stage lasting from about 2 weeks at 19-20°C to as long as 2 months at 100lloC (Templeman, 1936). In 1974 we surveyed 44 electrophoretically detectable, enzyme-coding loci in eight population samples from the Gulf of St. Lawrence, the Bay of Fundy, inshore areas of Maine and Massachusetts and canyons offshore of Long Island and Massachusetts (Tracey et aI., 1975). Continuous distribution and high potential for migration led us to expect uniform allelic frequencies. To our surprise we detected significant genetic differences among these populations, in particular a nearly fixed difference at a malic enzymecoding locus (Me) between Massachusetts inshore and Prince Edward Island samples. The alternative alleles characteristic of these two populations were found segregating at about equal frequencies in the offshore populations. To us, this was unambiguous evidence that the American lobster population is subdivided. [Shaklee's (1983) recent criticism of this interpretation, based on our reporting the enzyme in question to be a monomer rather than a tetramer as in other organisms, ignores phenotypic and population evidence that the observed electrophoretic variation has a genetic basis whether it is the "true" malic enzyme or not.] Statistical differences among allelic frequencies at other loci in our 1974 data set have since been pointed out by Burton and Feldman (1982), Burton (1983) and Shaklee (1983). Evidence that lobster populations are physiologically differentiated as well comes from extensive studies of vitellogenesis and molting. Working primarily with Massachusetts lobsters, we have demonstrated and routinely used a biphasic photoperiod regime to induce vitellogenesis and oviposition (Nelson et aI., 1983; Hedgecock, 1983; Nelson, 1986; Nelson and Hedgecock, 1985). On the other hand, Aiken and Waddy (1985a; 1985b) have recently reported that spawning of Prince Edward Island female lobsters is induced not by photoperiod cues but by spring seawater temperatures. Nelson (1986; Nelson and Hedgecock, 1985) suggests that both results may be correct and attributable to genetic and environmental (mainly temperature) differences between the two lobster stocks studied. In our laboratory, some Prince Edward Island females respond to the long day onset cue for secondary vitellogenesis, while others do not. Moreover, the European lobster, H. gammarus, pays not the least attention to photoperiod and this lack of response appears to be transmitted to F I interspecific hybrid offspring. These results suggest that variation in photoperiod response within and between lobster species may indeed have a genetic basis as has been shown for photoperiodic responses in diapausing insects. How might we reconcile genetic subdivision of the American lobster population, given the dispersal potential of its pelagic larval phase? A partial solution has emerged from recent studies of the role that the 1954 closing of the Strait of Canso might have had in the subsequent decline oflobster stocks off the Atlantic coast of Nova Scotia. Harding et ai. (1983) describe this region as "a 'fringe' zone ... requiring immigration of advanced larval stages or HEDGECOCK: PELAGIC LARVAL DISPERSAL AND GENE FLOW 553 juveniles to maintain stocks ... as the summer surface temperatures are in general too cool and the prey species too large to allow successful recruitment of the larval stages along the open coast." From studies of larval abundance in St. George's Bay (Gulf ofSt. Lawrence) and knowledge of flow rates through the Strait of Canso prior to 1954, Harding et al. (1983) estimate that the Gulf of St. Lawrence stock could have contributed up to 60% of the landings recorded in the 11 best years in the Chedabucto Bay (Atlantic coast) fishery. The presently depleted Atlantic stock is maintained by a low rate oflarval transport from the Gulf of St. Lawrence around Cape Breton Island, N.S. Plankton studies off the southern tip of Nova Scotia, on the other hand, reveal the arrival of larval stages that cannot have had time for local development at in situ temperatures; adult stocks there are probably maintained by the immigration of larvae produced along the northern edge of George's Bank. The population oflobsters along the eastern coast of Nova Scotia, therefore, is of mixed, migrant origin and is unable itself to contribute to lobster recruitment. Thus, despite a moderately long pelagic larval stage, Homarus americanus confronts, along the Atlantic coast of Nova Scotia, a formidable geographic (temperature, prey unavailability) barrier to larval dispersal between the Gulf of St. Lawrence and New England Atlantic populations. Whatever gene flow might have been possible between Gulf of St. Lawrence and New England stocks prior to the closing of the Strait of Canso was apparently insufficient to retard evolutionary divergence with respect to allozyme frequencies and reproductive responses to photoperiod and temperature cues. An alternative hypothesis, that divergence arose only after the closing, would require nearly complete lethality and dominance at the Me locus-for the 100 allele in the Gulf of St. Lawrence and for the 102 allele in the Massachusetts inshore area-in order to effect near fixation of these alleles in 20 years, a period spanning only about three generations. This seems unlikely, but testable by transplant experiments. DIVERGENCE OF BALANUS GLANDULA POPULATIONS Balanus glandula is a very abundant intertidal barnacle ranging over three eastern Pacific zoogeographic provinces, the Aleutian, the Oregonian and the Californian (Briggs, 1974). It releases nauplii which spend from 2 to 4 weeks in the plankton before settling mainly in late spring or early summer (Barnes and Barnes, 1956; Strathmann, 1982; J. Standing, pers. comm.). A survey ofallozyme variation in 25 population samples was conducted in 1976 and 1977 in order to estimate total genetic diversity and to partition this diversity into macro- and microgeographic components (Hedgecock, Standing, Herner and Nelson, in prep.). In contrast to decapods like Homarus, but in keeping with observations in other thoracican barnacles, B. glandula has very high levels of variation (Hedgecock et al., 1982); 70% of 27 loci studied are polymorphic and the average individual is heterozygous at about 21 % of these loci. We are able to compare allelic frequencies for seven enzyme polymorphisms among localities ranging from Kodiak, Alaska, to southern California but concentrated mostly in north-central California. Samples from south of Pt. Conception in the Californian Province have unique alleles at three loci (Got-2, Mpi and Pgi), but with the exception of the Got-297 allele which reaches a frequency of 0.2 in one southern Californian sample, these unique alleles are at low frequency. The Kodiak sample is distinctive only at the Pgi locus and possesses no unique alleles. Variation in allelic frequencies over all localities, including samples from the Aleutian and Californian Provinces, is slight, accounting for only 3.75% of the total genetic diversity in the species. This similarity of allelic frequencies over populations conforms with the ex- 554 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986 pectation that dispersing nauplii and cyprids provide a high rate of gene flow among sessile B. glandula populations. The slight, but measurable divergence between central and southern Californian populations is consistent with potential hydrographic or temperature barriers to larval dispersal in the vicinity of Pt. Conception (Pirie et al., 1975; Newman, 1979). Yet, without specific information on dispersal rates across this faunal boundary or on selection coefficients for allozymes, we cannot be sure where the balance between gene flow and diversifying selection lies. Despite apparent genetic homogeneity, statistical comparisons of allelic frequencies among localities reveal significant heterogeneities, often on a microgeographic scale. The most striking examples of this are significant differences at the Mpi locus among samples taken at different tidal heights from three vertical transects in the vicinity of Bodega Bay. In all three transects the 103 allele decreases and the 110 allele increases significantly in frequency in the middle of the barnacle zone. Otherwise, observed microgeographic variation for the most part shows no spatial patterning that might be correlated with gradients of environmental factors. Such heterogeneity must be explained in view of the likelihood that gene flow throughout the range, and certainly within a single region or province, is substantial. One explanation is that non-random, genotype-dependent mortality occurs after larval settlement, as convincingly demonstrated in Mytilus edu/is (Koehn et aI., 1976; Theisen, 1978; Koehn et al., 1980; Gartner-Kepkay et aI., 1983; cf. Koehn et aI., 1984). An alternative explanation, at least for the unpatterned variation seen in Balanus and the pulmonate gastropod Siphonaria (Johnson and Black, 1982), is that genetic heterogeneity among adult populations is a reflection of heterogeneity among larvae recruiting to those populations (Hedgecock et aI., 1982; Johnson and Black, 1982; 1984; Hedgecock, Standing, Herner and Nelson, in prep.). A preliminary test of the latter hypothesis was undertaken during the settling season of 1983 (Li, Hedgecock and Sly, in prep.). In late March, six 625-cm2 Masonite settling plates were attached to a beam positioned horizontally in the center of the barnacle zone on the Coast Guard dock in Bodega Harbor. Thereafter, at the end of each of the four succeeding monthly intervals, six settling plates were removed and replaced by fresh plates. Because the newly settled barnacles were too small for electrophoresis, settling plates removed after one month's exposure were taken to the laboratory and held in running, filtered sea water; brine shrimp nauplii were fed daily to the attached barnacles. Half of the settling plates were harvested for electrophoretic analysis on 1 August, while the remainder were harvested on 23 September. Samples of 120 individuals from each plate (a total of 2,880 specimens) were examined at the Got-1, Got-2, Mpi, Pep, and Pgi polymorphic loci. Unfortunately, in this pilot experiment, treatment (month of exposure to larval recruitment) became confounded with length oftime barnacles were reared in the laboratory prior to analysis. The staggered harvest schedule fortunately does permit two independent comparisons between treatment groups which settled one to two months apart but which differed by only eight days of laboratory rearing. Analysis of cross-classified categorical data (ACCCD; Fienberg, 1980) reveals complete independence of allelic frequency, position of settling plate in the linear array and exposure interval, at all five loci for these experimental groups (an example of results for Mpi is given in Table 1). Thus, larval cohorts recruiting at different times during a settling season are genetically homogeneous and appear to constitute random samples from the species gene pool. Interestingly, the frequency of the MpiJOO allele increases significantly with the length of laboratory HEDGECOCK: Table I. 555 PELAGIC LARVAL DISPERSAL AND GENE FLOW Goodness-of-fit tests for loglinear models (Fienberg, 1980) of Mpi allele frequencies among Balanus glandula recruiting to settling plates in Bodega Harbor, California, in 1983. (Data from Li, Hedgecock and Sly, in prep.) First two sets of columns test differences between groups settling in different months and reared in the laboratory for about the same number of days; month [A], allele frequency [B] and replicates [C] are independent (no significant departures). The third set of columns tests differences between 98 and 150 days of rearing following settlement in April; best fit is to model 6, suggesting an interaction of replicates [A] and allele frequency [B] is independent from an interaction between allele frequency and growout time [C]. * = P < 0.01 April 98 d I 2 3 4 5 6 7 8 [A][B][C] [AB][C] [AC][B] [BC][A] [AC][BC] [AB][BC] [AB][AC] [AB][BC][AC] culture as shown ACCCD of earlyIn the laboratory, specific mortality vs. June 90 d May vs. July 67 d 59 d 98 d April v,. 150 d df G df G df G 22 18 20 14 12 10 16 8 36.24 32.95 36.22 23.37 23.37 20.08 32.94 20.04 22 18 20 14 12 10 16 8 18.62 16.33 18.24 13.16 12.78 10.87 15.95 10.48 22 14 20 18 16 10 12 8 46.19* 19.64 46.19* 35.72 35.72* 9.17 19.64 8.98 by Spearman rank correlation (rs = 0.76, P < 0.05) and by and late-harvested subsets within treatment groups (Table 1). and apparently in the field as well, non-random, genotypemodifies the genetic composition of recruiting populations. DIFFERENTIATION OF POPULATIONS DESPITE GENE FLOW Although early evidence seemed to show a correspondence between larval dispersal and genetic differentiation of geographically separated populations (reviewed by Gooch, 1975), recent critical reviews (Burton and Feldman, 1982; Burton, 1983) have shown the relationship to be less than clear cut. Marine invertebrates whose larvae are not planktonic do show greater geographic variation in allelic frequencies than species with such larvae. For many species without larval dispersal the distribution ofallozymes is frequently that seen in population models of low gene flow-alleles found in only a few localities reach high frequencies in those particular local populations (Slatkin, 1981). On the other hand, most species having planktonic larvae (cf. Marcus, 1977) show allele frequency distributions characteristic of high gene flow-alleles reaching high frequency are widely shared among localities. Beneath this apparent genetic homogeneity, nevertheless, lies considerable heterogeneity of population structure. As pointed out by Burton (1983), uniformity of gene frequencies has been convincingly demonstrated in surprisingly few species with pelagic, planktotrophic larvae (Berger, 1973; Gooch et aI., 1972; Snyder and Gooch, 1973; Winans, 1980). Many more studies of such organisms [reviewed by Burton (1983; 1986) and discussed below] have demonstrated significant geographical variation in gene frequencies. Indeed, Burton (1983) concludes, " ... the genetic structure of natural populations of marine invertebrates cannot be reliably inferred from their apparent dispersal capacities. This conclusion contrasts with those of Gooch (1975) and Crisp (1978), but seems justified by the data reviewed .... " Failure to observe genetic homogeneity consistently among conspecific populations dispersing primarily by means of pelagic larvae may have several causes: (1) Actual levels of gene flow may be less than presumed because of physical 556 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986 or biological barriers to larval dispersal. Differentiation of Gulf of St. Lawrence and Atlantic populations of Homarus americanus with respect to allozyme frequencies and reproductive physiological ecology illustrates genetic consequences of environmental restriction upon larval dispersal. Populations of adult lobsters are continuously distributed along the continental shelfthroughout New England, around Nova Scotia and into the Gulf of St. Lawrence. Lobster larvae are capable of dispersing relatively long distances (1D's to 1OD'sof kilometers?), yet sea surface temperatures and dearth of suitable prey along the eastern Nova Scotian shelf apparently restrict the exchange oflarvae between Atlantic and Gulf stocks. This barrier might have remained unrecognized were it not for the closing of the Strait of Canso and subsequent analysis of the decline in abundance of lobsters along the Scotian shelf (Harding et aI., 1983). The evolution of important population differences appears to have accompanied a natural geographical isolation of North American lobster stocks that must date to the end of the last glaciation. That such geographical isolation has resulted in allopatric divergence oflobsters on a larger scale is suggested by the likelihood that earlier separation of western and eastern Atlantic lobsters by Pleistocene glaciation allowed the divergence of the American and European species of Homarus (Hedgecock et aI., 1977). Capacity of the pelagic larva to affect its own dispersal might also act as a barrier' to gene flow. Burton and Feldman (1982) suggest that larval behavior and swimming capability might mean the difference between a population structure predicted by a model of passive dispersal and a more complicated structure maintained by patterns of active dispersal. The patchy distribution of genetic variation in the intertidal copepod Tigriopus califomicus strongly suggests a lack of gene flow between the rocky outcrops on which they occur, owing perhaps to behavioral adaptations that may prevent them from being washed off and dispersing among outcrops separated by as little as one kilometer (Burton, 1983; 1986). More comparative data are needed on the population structures of marine invertebrates with and without strong swimming larvae to test Burton and Feldman's thesis. How often barriers to larval dispersal have significant genetic and evolutionary consequences for marine invertebrates remains to be answered. Genetic analysis alone is usually insufficient to decide whether population differentiation has resulted primarily from a restriction oflarval dispersal or from diversifying natural selection. Documentation of actual exchange via larval dispersal remains a significant challenge in marine biology. (2) Conflicting results regarding the differentiation of conspecific populations may be due to statistical artifacts and methodological problems in quantifying population structure. The geographical pattern of allele frequency variation may differ from locus to locus, particularly if the pattern or intensity of selection varies for each gene (Christiansen and Frydenberg, 1974). Even in the absence of selection the variance of gene frequencies over subpopulations has, itself, a large sampling variance, especially when estimated from a small number of allozyme loci (Nei and Chakravarti, 1977; Nei et aI., 1977). Rigorous analysis of population structure in most species that have been studied to date is precluded by inadequate sampling of loci. Another problem with earlier studies is the inference of genetic similarity from morphological similarity (see for example Scheltema, 1971). The biochemical systematics literature now contains numerous examples of cryptic sibling species in a wide variety of marine invertebrate taxa (sea anemones, Bucklin and Hedgecock, 1982; sea cucumbers, Manwell and Baker, 1963; copepods, Volkman-Rocco and Battaglia, 1972; Volkman-Rocco, 1973a; 1973b; Volkman et aI., 1978; polychaetes, Grassle and Grassle, 1976; Nicklas and Hoffman, 1979; gastropods, Ber- HEDGECOCK: PELAGIC LARVAL DISPERSAL AND GENE FWW 557 ger, 1977; Murphy, 1978; Mastro et aI., 1982; Hoagland, 1984; bivalves, Skibinski et aI., 1978; cf. Gosling, 1984; Koehn et al., 1984; barnacles, Hedgecock, 1979; Dando and Southward, 1980; 1981; and crabs, Salmon et al., 1979; Bert, 1985). The converse situation, biological species that are morphologically polytypic, has been demonstrated in marine invertebrates by studies of electrophoretic similarity, tests of interfertility or studies of developmental plasticity (limpets, Gaffney, 1980; Giesel, 1970; Murphy, 1983; gastropods, Struhsaker, 1968; Palmer, 1984; 1985). The problem of morphologically defined taxa is discussed below in connection with the evidence for long-term evolutionary consequences of larval dispersal. (3) Differentiation of conspecific populations of marine invertebrates having pelagic larvae may arise from differential survival or mating success of immigrants after settlement (Burton and Feldman, 1982; Burton, 1983). That differentiation of conspecific populations of benthic marine invertebrates by natural selection can occur has been well documented, particularly for Mytilus edu/is (Koehn, 1975; Koehn et aI., 1976; 1980; 1984). A stable cline in aminopeptidase-I (Lap) allozyme frequencies over Long Island Sound populations is maintained by selective mortality of recruits from differentiated oceanic populations (Koehn et al., 1980). By contributing to intracellular free amino acid pools, the protein-catabolizing aminopeptidase-I plays a critical role in cell volume regulation and response to osmotic stress. Differential mortality among Lap genotypes has been traced to genotype-specific differences in the activity of an enzyme governing physiologically adaptive reactions (Hi1bish and Koehn, 1985). Although a complete description of the relative fitnesses of oceanic recruits into Long Island Sound awaits study of reproductive success-selective mortality continues at sizes greater than the minimum size for maturity (Seed, 1969)-larval dispersal between Atlantic and Sound mussel populations clearly cannot be called adaptive gene flow. The situation in Mytilus is analogous to many examples in ecological geneticsindustrial melanism in lepidoptera (Clarke and Sheppard, 1966; Ford, 1964), shell polymorphisms in terrestrial molluscs (Cain, 1983), and differentiation of plant populations across toxic soil boundaries at mines (Jain and Bradshaw, 1966; Antonovics and Bradshaw, 1970). Interestingly, diversifying selection is more effective against gene flow when it acts on recruiting larvae or seeds before mating than when it acts on immigrant gametes following their union with resident gametes (Antonovics, 1968). How often locally adaptive differentiation of populations occurs in the face of substantial gene flow is yet to be determined. For Balanus glandula we have evidence that gene frequencies among recruits over a four-month settling season are homogeneous; nevertheless, adult gene frequencies are statistically heterogeneous on micro- and macrogeographic scales. Thus, differential mortality after settlement appears to alter significantly the genotypic composition of local adult barnacle populations. This conclusion is supported by rapid changes in allelic frequencies of laboratory-reared recruits. In contrast, fine-scale, ephemeral patchiness of gene frequencies among adult populations of the pulmonate limpet Siphonaria jeanae appears to be explained by temporal variation in the settlement patterns and genetic composition of recruits (Johnson and Black, 1984). Since recruits at anyone settlement are genetically homogeneous over sites and geographical variation in adult frequencies appears too limited to account for the differences among recruiting cohorts, Johnson and Black (op. cit.) conclude "that selective mortality, either in the plankton or soon after settlement, is the major determinant of allelic frequencies in recruits" and that "genetic changes in recruits occur in spite of, rather than resulting from, planktonic dispersal." 558 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, ADAPTIVE SIGNIFICANCE OF PELAGIC 1986 LARVAL DISPERSAL Diversifying selection operates on different spatial and temporal scales which determine whether gene flow is adaptive (Levins, 1964; Strathmann, 1982). To the extent that selection coefficients vary temporally and spatially on fine scales, as they apparently do in Siphonaria, larval dispersal may well be adaptive, damping genetic response to local, ephemeral environmental conditions. Johnson and Black (1984) conclude, "the importance of gene flow through planktonic larval dispersal is not that genetic divergence cannot occur. Rather, divergence cannot accumulate, but must be renewed each generation." Much of the unpatterned, microgeographical variation in allozyme frequencies of Balanus glandula may also fall into this category. To the extent, however, that selection coefficients vary spatially on scales coarser than the individual ranges of adult benthic marine invertebrates, for example over intertidal zones, along estuarine gradients or across biogeographic boundaries, continual dispersal oflarvae between areas will reduce fitness in all areas (Levins, 1964). Under these circumstances one expects the evolution of barriers to gene flow (Thoday and Gibson, 1962; McNeilly and Antonovics, 1968). Again, our best examples of coarse spatial patterning of genetic differentiation in the face of gene flow are in Mytilus edu/is (Koehn et al., 1980; Theisen, 1978). There is no experimental evidence yet for incipient barriers to larval dispersal or gene flow between estuarine and oceanic mussel populations. Nevertheless, similarity of Lap allelic frequencies between recruits and residents of inner Long Island Sound is consistent with larval retention or exclusion of immigrating oceanic recruits. Moreover, a separate genetic prediction might be tested. Dominance at a locus under directional or diversifying selection enhances the effectiveness of phenotypic selection, and where selection gradients are steep with respect to gene flow, dominance acts as an isolating barrier (Antonovics, 1968). If the dominance recently demonstrated for the Lap locus in Mytilus (Hilbish and Koehn, 1985) has evolved in response to the loss of fitness owing to larval dispersal across a steep selection gradient, we might predict the degree of dominance to decline with distance from contact between estuarine and oceanic populations. The Mytilus example strongly supports the viewpoint that gene flow via dispersing pelagic larvae can be maladaptive with respect to spatial patterns of environmental variation and diversifying selection. It remains to be determined whether geographic patterns of genetic variation in other marine invertebrates having pelagic larvae can be similarly interpreted. The evidence for selection in other species is suggestive, but not conclusive. In the case of Balanus glandula, for example, we need data on the gene frequencies of cyprids recruiting to either side of the biogeographic boundary at Pt. Conception and to various tidal levels in order to interpret observed macro- and microgeographic patterns of genetic differentiation. The development in studies of Mytilus, Siphonaria, and Balanus of protocols for comparing recruits and residents in order to test the relative importance of diversifying selection versus gene flow offers considerable hope for resolving the population genetic role of pelagic larvae. If the large amount of selective mortality needed to accomplish genetic differentiation despite high gene flow is a price paid for having a pelagic larva, what are the benefits that favor the evolution of this life history phase? One benefit might be increased survival by migration to nursery habitats that are ecologically favorable for early development (Strathmann, 1982). Positive selection for migration to a distinct nursery habitat would have the accidental consequence of increasing gene flow among populations; losses due to differential survival could HEDGECOCK: PELAGIC LARVAL DISPERSAL AND GENE FLOW 559 either be balanced by evolution of increased fecundity or cut through the development of reproductive isolation. There is clear need for expanding our empirical knowledge of the adaptive significance of pelagic larvae. Fortunately, research protocols for testing life history theory for marine invertebrates are evolving rapidly in several areas of population biology. EVOLUTIONARY SIGNIFICANCE OF PELAGIC LARVAL DISPERSAL Exciting new information concerning the evolution of marine bivalve and gastropod molluscs has come from recent paleontological studies of species whose larval life histories may be inferred from shell morphology (Jablonski and Lutz, 1983; Jablonski, 1986). These authors convincingly demonstrate that Late Cretaceous gastropods with planktotrophic larval development have greater geographic and stratigraphic ranges than gastropods with lecithotrophic larval development. Jablonski (1986) interprets these distributional data, in part, as evidence that the mode of larval development influences the general, background tempo and mode of speciation and extinction in gastropods. He argues further that an "irreducible species-level" difference between the population genetic structures of the planktotrophic and nonplanktotrophic modes is the cause of this macroevolutionary pattern. Nonplanktotrophs, with their limited dispersal capabilities and genetically differentiated species, are most likely to be subject to shifting balance mechanisms [with reference to "Wright 1931, 1982 and many other papers"], whereas the more widely-dispersing planktotrophs tend to be genetically more homogenous over evolutionary timescales, ruling out a shifting balance process (Jablonski, 1986). To continue with Jablonski's (1986) syllogism: (1) "For marine gastropods, genetic population structure is strongly influenced [as described above] by modes oflarval development, which differ in dispersal capability." (2) "There is variation among species for [dispersal] traits. These traits are heritable at the species leve1." (3) Therefore, " ... species having a given mode of development tend to have similar geologic durations, speciation rates and extinction rates." That is, nonplanktotrophic species because of their subdivided population structures appear and disappear more rapidly and occupy more limited geographic distributions in the fossil record than planktotrophic species. I believe this argument to be false for two reasons. First, the fossil taxa studied by Jablonski and co-workers are necessarily defined on the basis of shell characters alone. As cited above, biochemical genetic studies reveal the rather frequent occurrence of morphologically cryptic, sibling species in marine invertebrates. Many of these cases are widespread species having planktotrophic larvae, such as Mytilus, Littorina, and Chathamalus. On the other hand, controlled laboratory matings of the gastropod Thais emarginata show that a striking dimorphism of shell sculpture is under simple genetic control and subject to environmental modification through phenotypic plasticity (Palmer, 1985). While both shell sculpture and color vary over the geographic range of this species, as might be expected just on the basis of its lecithotrophic mode of larval development, fertility and viability in interpopulation crosses are consistent with a high degree of genetic similarity among geographically separated populations (Palmer, 1984). Were it found in the fossil record, a shell sculpture dimorphism similar to that of T. emarginata might well be misinterpreted as evidence of two species with the restricted and nested ranges that Jablonski finds typical of species with lecithotrophic development. Thus, the assumption that speciation and extinction rates 560 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986 can be reliably estimated from fossil distributional data is falsified by neontological genetic evidence that morphological change need not be coupled with speciation. The severity of this taxonomic problem for Jablonski's argument is best appreciated by inspecting the observed distributions of stratigraphic ranges for planktotrophs and nonplanktotrophs (fig. 4, Jablonski, 1986). If just a few of the planktotrophs were split into shorter-lived species and just a few of the nonplanktotrophs were lumped into longer-lived species, the two histograms would easily be rendered statistically indistinguishable. Second, even if we could accept the fossil data as valid evidence of speciation and extinction rates, Jablonski's major premise that the dichotomy in mode of larval development results in qualitatively different population genetic structures is also not supported by the neontological evidence discussed in the previous section. Population differentiation of living marine invertebrates is caused primarily by diversifying selection, acting as a function of the spatial structure of environmental heterogeneity and without regard to the level of gene flow afforded by larval dispersal. Despite these criticisms, I agree with Jablonski that the macroevolutionary patterns of morphological change in fossil planktotrophic and lecithotrophic gastropods requires "hierarchical" explanation. Differences in the tempo and mode of phenotypic evolution for the two groups cannot be reduced to a difference in population genetics. An alternative explanation, however, may be derived from consideration of the evolutionary forces acting upon shell morphology. Suppose that rates of speciation and species extinction are roughly equivalent for the two groups, but that detection of these events at the morphological level differs. We might, for example, postulate that there is a slight bias against the evolution of new shell morphologies in planktotrophs because a major selective pressure on this trait, predation by crabs, tends to show fine-grained temporal and spatial variation (Menge, 1976; Vermeij, 1982) while selective pressures on physiological characters, such as temperature or salinity tolerances, tend to follow coarse-grained spatial patterns. Loss of fitness from gene flow across steep thermal or salinity gradients might drive the evolution of reproductive isolation between morphologically very similar but physiologically different populations. For nonplanktotrophs, we might postulate a slight bias towards the expression of new morphologies without speciation. Low levels of gene flow in these species might indeed allow genetic or phenotypic responses to local selection pressures on shell morphologies, but without direct selection for reproductive isolation, geographically separated populations might remain fully interfertile as in Thais emarginata (Palmer, 1984). Discrepancies in rates of evolution at different phenotypic levels is an accepted tenet of evolutionary biology which has been confirmed at least for bivalve molluscs (Hedgecock and Okazaki, 1984). CONCLUSION The weight of genetic evidence on population structure in marine invertebrates having pelagic larvae supports Strathmann's (1982) contention that the shortterm evolutionary significance of a pelagic larval phase is not likely to be dispersal for gene flow. There is no doubt that dispersal and gene flow are greater in species with planktotrophic larvae than in species with nonplanktotrophic larvae. But pelagic larvae may face unknown barriers to dispersal and even when they do reach distant populations their contributions to those populations may be minimized by reduced viability or fecundity. For coarse-grained spatial patterns of diversifying selection, gene flow is clearly maladaptive, and it may well stimulate HEDGECOCK: PELAGIC LARVAL DISPERSAL AND GENE FLOW 561 the formation of barriers to larval dispersal. Gene flow by pelagic larval dispersal is perhaps better interpreted as an accidental by-product of selection for a migration dictated by developmental, physiological, or ecological constraints on early life history stages. The argument that macroevolutionary patterns ofplanktotrophs differ from those of nonplanktotrophs because of differences in population genetic structure is found wanting. An alternative explanation for differences in the tempo and mode of morphological evolution in Late Cretaceous gastropods is that shell sculpture is determined largely by selective predation which varies on fine-grained temporal and spatial scales. The interaction of such a selective pressure with population structure has led to an uncoupling of morphological change and speciation. ACKNOWLEDGMENTS Several workshop participants made constructive criticisms, but special thanks go to Professor R. Strathmann for his thought-provoking written review. Dr. E. Hutchinson provided valuable editorial assistance in the eleventh hour. Lobster research was supported by the California Sea Grant College Program. LITERATURE CITED Aiken, D. E. and S. L. Waddy. 1985a. The uncertain in/luence of spring photoperiod on spawning in the American lobster, Homarus americanus. Can. J. Fish. Aquat. Sci. 42: 194-197. -and --. 1985b. 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