Download Is gene flow from pelagic larval dispersal

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
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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-
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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
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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."
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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.
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DATEACCEPTED: February 10, 1986.
ADDRESS: University of California, Davis, Bodega Marine Laboratory, P.O. Box 247, Bodega Bay,
California 94923.