Download What controls the type of larval development? Summary statement

BULLETIN OF MARINE SCIENCE, 39(2): 61~22,
LARVAL INVERTEBRATE WORKSHOP
1986
WHAT CONTROLS THE TYPE OF LARVAL DEVELOPMENT?
SUMMARY STATEMENT FOR THE EVOLUTION SESSION
Richard R. Strathmann
ABSTRACT
Length of the planktonic larval period can determine dispersal distances of sedentary
benthic animals and thereby influence genetic variation within and among subpopulations,
accumulation or elimination of deleterious recessive genes, and adaptation to local conditions.
These microevolutionary changes, together with possible differences in geographic range, may
influence speciation and extinction rates, If length of planktonic period is important to
evolution, then how does length of planktonic period evolve?
Types of embryonic and larval development (benthic or planktonic, feeding or non-feeding)
determine duration ofthe planktonic period. Therefore conditions controlling types ofIarval
development ultimately control evolutionary processes for descendent lineages insofar as
dispersal influences these processes. Here I list 10 hypotheses on persistence of types of
development and transitions between types of development. These conditions include trades
between rate of early development, rate of early growth, and risks from benthic and planktonic
predators. The size of adults and larvae, body plans of adults, body plans and feeding mechanisms of larvae, and internal fertilization determine the form of these trades. Transitions
between types of development are restricted by a bias against recovery of a feeding larval
stage and stabilizing selection for local adaptive optima. Advantages oflong distance dispersal,
differences in reproductive effort, and adaptations for larval settlement have little effect on
type of larval development and duration of planktonic periods.
EVOLUTIONARY CONSEQUENCES OF TYPE OF LARVAL DEVELOPMENT
Planktonic feeding larvae of ben thic animals usually disperse widely, whereas
dispersal distances are usually very short when embryonic and larval development
is entirely benthic or when released larvae are nearly competent to settle. Mode
oflarval development is thus expected to influence evolutionary processes through
its influence on dispersal distances.
Conference Papers
Papers in the evolution session explored the dependence of both microevolutionary and macroevolutionary processes on the type of embryonic and larval
development. Taken together they gave the following picture. The type of embryonic and larval development affects dispersal and hence gene flow in species
with sedentary adults (Hedgcock, this issue; Burton, this issue; Grosberg, unpublished). Long distance larval dispersal is generally correlated with more genetic
variation at a site and less genetic variation among sites, though selection within
each generation may result in variation among sites despite long distance larval
dispersal (Hedgcock, this issue). Very short dispersal distances for larvae are often
associated with less genetic variation within sites and sometimes more variation
among sites. Variation among sites can be in the form of different coadapted gene
complexes or different mechanisms of coping with local conditions. This may
result in outbreeding depression when animals from more distant subpopulations
are interbred (Burton, this issue; Grosberg, unpublished). Kin recognition or histocompatibility permitting colony fusion may provide benefits to animals with
very short distance larval dispersal (Grosberg, unpublished; Jackson, this issue).
On a larger time scale, feeding development (and long distance dispersal) may
result in greater geographic range, greater species longevity, lower speciation rates,
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and lower extinction rates than species with non-feeding larvae (Jablonski, this
issue). Thus type of larval development may affect differential speciation and
extinction, or species selection, but larval development may affect differential
speciation and extinction differently at times of massive world-wide extinctions
(Jablonski, this issue; Valentine, this issue). Type oflarval development may have
profound evolutionary consequences through its influence on dispersal.
General Predictions on Evolutionary Consequences
Though there is disagreement on the generality of some of these evolutionary
consequences of larval dispersal, my impression from the conference papers and
from previous work (Burton and Feldman, 1982; Hansen, 1980; Jablonski and
Lutz, 1983; MacKay and Doyle, 1978; Scheltema, 1977; Shuto, 1974) is that most
studies can be fit into a consistent scheme.
With little or no larval dispersal and sedentary adults, there is reduced gene
flow so that genetic drift, local directional selection, or local inbreeding result in
decreased genetic variation within local subpopulations and increased genetic
variation among local subpopulations. Specific adaptations to local conditions or
local coadapted gene complexes may result. Under these circumstances deleterious
recessives are expressed and eliminated. Thus inbreeding depression is reduced
and there may be outbreeding depression. As a consequence of outbreeding depression, additional mechanisms for retaining offspring or restricting outcrossing may
evolve. Larval selection of sites near parents or siblings is one suggested possible
outcome. Lower frequency of deleterious recessive genes can affect breeding systems and sex allocation (Charlesworth and Charlesworth, 1981; Charnov, 1982).
For example, simultaneous hermaphrodites with partial self fertilization and reduced male allocation may be at a reproductive advantage relative to obligate
outcrossers when inbreeding depression is reduced (Strathmann et aI., 1984). The
isolation and divergence of local populations may result in increased speciation
and decreased geographic ranges. Species living at and specialized for a narrower
range of sites may also have higher extinction rates.
With a longer planktonic larval stage there is increased gene flow. Selection
may produce genetic variation among local subpopulations each generation, but
genetic variation among subpopulations is decreased and genetic variation within
subpopulations is increased. Generalist traits may be favored. With high outcrossing, deleterious recessive genes are accumulated. The increased costs of inbreeding result in the evolution of mechanisms that ensure outcrossing and in
barriers to the evolution of selfing.
These correlations between type of larval development and evolutionary processes are not perfect. Larvae are not the only means of dispersal for benthic
invertebrates; larval behavior affects dispersal; dispersal is not the only factor
determining genetic exchange; and other factors than genetic exchange affect the
genetics of populations. Nevertheless, this outline does express some of the expected genetic and evolutionary consequences of type of larval development.
Further studies will test the generality of these predictions and causes of exceptions
to these predictions. Differences in environment, ancestry, and traits other than
type of larval development are certain to force modifications of this scheme.
CAUSES OF TYPES OF LARVAL DEVELOPMENT
If type of larval development is a major determinate of evolutionary processes
among benthic marine animals, then conditions controlling the type of larval
development control evolutionary processes in the clade. Why does a species have
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1986
benthic or planktonic development? A feeding or non-feeding larva? Factors determining type of larval development received less attention at this conference.
Conference Papers
Shifts from feeding to non-feeding larval development have been found in
Cretaceous and Tertiary molluscs, but not the reverse (Jablonski, this issue). Then
where and when, do feeding larval forms originate? The feeding mechanism of
veligers might be inherited from pre-molluscan ancestors with feeding trochophore
larvae, a suggestion that pushes the problem back into the origins of the protostome
phyla. On the other hand, early Cambrian molluscs were very small, a trait that
today is often associated with absence of a feeding larval stage (Chaffee and
Lindberg, this issue). If the dawn-mollusc lacked a feeding larva, feeding veligers
evolved at least twice in the Mollusca, and one wonders how.
Jackson suggested that sites near the parent or siblings are more likely to be
favorable for many colonial animals and that selection for short dispersal distance
has influenced the evolution of brooding and larval development for colonies.
Because brooding and short dispersal distances are also common among solitary
benthic animals with small adult size, I would reverse the interpretation of causes.
A large mass of cells requires a circulatory system; a large mass of embryos lacks
a circulatory system. Therefore a large surface may be required to hold and
ventilate embryos. It is small solitary animals and colonies with small repeated
members that have large surface areas relative to their body mass and fecundity.
This suggests that colonies with high surface areas are preadapted for retention
and ventilation of brooded embryos, that brooding results in short dispersal distances and limited gene flow, and that adaptations to local conditions or proximity
of kin are the result of brooding and short dispersal distance, not its cause.
Valentine argued that energy available to adults influences the evolution oftype
of larval development, and I found myself in disagreement with this hypothesis,
at least as I understood it. If one type of development yielded higher returns in
benthic juveniles per energy allocated to reproduction, then it would always be
favored unless there were a compensating advantage to another type of development. These compensating advantages must depend on other factors. Transitions between types of development or differential success oflineages with different
types of development could result from shifts in any of several factors, not just
energy limitation. If decreased parental investment per offspring results in increased vulnerability of offspring, as in Vance's (1973) models, a calorie allocated
to reproduction could result in similar numbers of juveniles whether the development was by way of planktotrophic, lecithotrophic, encapsulated, or brooded
stages. Also, no consistent relation has been found between type of larval development and reproductive effort (as reproductive output relative to adult biomass
or energy expenditure).
General Predictions on Causes of Types of
Larval Development
Models for the evolution of planktonic and benthic development and of feeding
and non-feeding larval development have predicted shifts in mode of development
in response to different combinations of development rates, planktonic and benthic mortality rates, relative vulnerability of different stages to predators, costs of
protective capsules or brood protection, availability of food for larvae, and advantages of dispersal or risks ofloss from favorable habitat (Caswell, 1981; Christiansen and Fenchel, 1979; Grant, 1983; Palmer and Strathmann, 1981; Pechenik,
STRATHMANN:
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1979; Strathmann, 1974; Vance, 1973). Regular trends in these variables could
be associated with season, geography, and habitat. For example, Thorson (1950)
suggested that variations with latitude or depth in the frequency of types of
development are caused by shifts in development rates and availability of food.
Highsmith (1985) suggested that latitudinal shifts in mortality rates could account
for the same trend; higher mortality rates in the benthos or lower mortality rates
in the plankton at low latitudes could also account for Thorson's rule. In all these
discussions, the optimal response to present conditions is the basis for predictions
on type of larval development. This emphasis is justified because populations
must persist in the short run of a few generations before long term processes
involving differential speciation and extinction may influence type of larval development.
Within a given region, differences in size and body plan account for much of
the variation in types of larval development. The following hypotheses are extracted from published models and comparative observations. Most have long
histories. They are deliberately simplified so that they can be more easily criticized
and tested. Explication and qualification are minimal because I have reviewed
some of these topics at greater length elsewhere (Strathmann, 1982; 1985; 1986).
1. The plankton is generally safer than the epibenthos for unprotected small
animals and offers more food and oxygen than the interstitial benthos. This is
why unprotected larvae are usually planktonic.
Unprotected embryos (not brooded or encapsulated) are more vulnerable to
predators than are larvae.
2. A major function of a feeding larva is to convert a small egg into a larger
juvenile at metamorphosis. A reduction in initial larval size permits higher fecundity, but imposes risks from a longer period of larval feeding. The trade of
decreased initial size against increased larval mortality depends on food supplies
and the larval form.
Because food supplies are often limiting, growth rates of larvae frequently depend on the rate of clearing a volume of water for food and on the range of food
items that can be captured. Clearance rate and sizes of food captured increase
with larval size, and this relationship depends on the body plan of the larva and
the feeding mechanism of the larva (Strathmann, 1986). The effect of reducing
egg size (parental investment per offspring) is therefore different with different
types of feeding larvae. Similarly, vulnerability to predators may differ among
larval forms. Because larval forms are conservative and characteristic of different
taxa, the trades between fecundity, growth, and survival will differ among taxa
in ways that affect the length of the planktonic larval period and thus the evolution
of lineages within the taxon.
A similar argument concerns size at metamorphosis. If the body plan and habitat
permit a smaller size at metamorphosis, either the period of larval feeding can
be shorter (which decreases larval mortality) or the egg size can be reduced (which
increases fecundity) (Strathmann, 1977).
3. The egg capsules that provide the most effective defense for benthic eggs
cannot be penetrated by sperm. Internal fertilization is a precondition for the
evolution of highly predator resistant encapsulation.
Encapsulation requires high surface areas for ventilation, and this increases
costs of defensive encapsulating materials (Strathmann and Chaffee, 1984). Encapsulation can retard development, and this reduces the gains from a lower
instantaneous rate of mortality (Chaffee and Strathmann, 1984).
4. Embryos brooded on or in the parent's body must be both retained and
ventilated. For many types of solitary adults, fecundity increases disproportion-
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1986
ately with surface area as adult size increases, so large animals are less capable of
successfully brooding all the offspring that they can produce (Strathmann and
Chaffee, 1984; Strathmann and Strathmann, 1982; Strathmann et aI., 1984). This
is why small adults and colonies with small zooids and high surface area are often
brooders, and few large solitary animals are brooders. Crustaceans include major
exceptions, but for the Malacostraca, limbs and relatively large eggs provide
unusually effective mechanisms for retention and ventilation of embryos. Thus
this constraint also depends on body plan.
5. Feeding larval forms originated long ago and have been very conservative.
A feeding larval stage is often lost in a lineage but rarely regained. The biased
transition to a non-feeding larva or no larval stage results in large clades lacking
a feeding larval stage and therefore lacking routine long distance dispersal (Strathmann, 1978a; 1978b).
6. More recently acquired larval feeding mechanisms (or at least those of more
limited taxonomic distribution) consist in part of formerly juvenile characters
now expressed in the planktonic larval stage (Jagersten's "adultation" or more
generally "heterochrony"). Alternatively, a formerly benthic juvenile stage may
become planktonic with little modification. In either case, the usual result is a
larger egg and larger size at initial feeding than occurs with the probable ancestral
larval form (Schroeder and Hermans, 1975; Strathmann, 1978a; 1978b).
7. The form of relationships between egg size, development time, growth, and
mortality rates also creates barriers to transitions in type of development. Simple
models of these trades result in adaptive troughs between separate adaptive peaks
under a wide range of conditions (Caswell, 1981; Grant, 1983; Vance, 1973).
Stabilizing selection can maintain mode of development at a lower adaptive peak
until a change in conditions eliminates the trough between peaks.
Published models have not produced more than two stable developmental types
for a given set of conditions, but among co-occurring species one finds continua
from entirely benthic to largely planktonic development or broad variation in egg
sizes and periods oflarval feeding. The published models can include such multiple
states by the assumption of different conditions for each species, but the existence
of nearly continuous variation among co-occurring species suggests deficiencies
in the models.
8. Reproductive effort (reproductive output per adult biomass or total energy
expenditure) is not a constraint on type of larval development. If one mode of
development gave higher returns per effort, all animals should have that mode
of development.
Though low reproductive effort and long life may result from varying recruitment associated with a longer planktonic larval stage, reproductive effort is not
closely com,lated with larval planktotrophy in interspecific comparisons (Grahame, 1982; Hughes and Roberts, 1980; Strathmann, 1985).
9. Selection among individuals does not favor large scale dispersal. Costs to
large scale dispersal involve loss from favorable sites.
Ova or embryos are released into the plankton when the size, body plan, or
activities of the parent constrain brood capacity or when external fertilization
constrains protective encapsulation. Long precompetent larval periods are associated with feeding and growth. Large scale dispersal is an accidental byproduct
of a planktonic period that provides adequate ventilation or relatively greater
safety or growth rate for small offspring.
10. Specific adaptations for settlement have had little influence on evolution
of planktonic period.
STRATHMANN:
SUMMARY STATEMENT ON EVOLUTION
621
A short planktonic period is a precondition for settlement adapted to kin or
local conditions, not a result of it.
Todd and Doyle's (1981) settlement-timing hypothesis is an interesting idea
but because it requires close constraints on optimal times of both spawning and
settlement, the hypothesis has potential application to few groups.
Some larvae have a two stage metamorphosis in which a feeding precompetent
stage metamorphoses to a competent larval stage, often non-feeding, that settles
and then metamorphoses to a benthic juvenile. This is an adaptation for settlement
but does not greatly affect total planktonic period.
These are plausible hypotheses on what determines differences in larval development for co-occurring species. They are not the ten commandments. Finding
basic flaws in each hypothesis is an exercise left for the reader. In most cases, this
will require better comparative data. I emphasized influences associated with body
plans and problems in functional morphology because they are important but
unfashionable topics of study. I would argue that trends associated with environment or habitat result largely from differences in development time, larval growth
rates, and risks to embryos and larvae from benthic and planktonic predators,
with loss from long distance transport of larvae possibly also playing a role. For
a given environment and habitat, functional constraints associated with conservative structures influence the type of development and thereby influence the
evolutionary processes in a clade.
ACKNOWLEDGMENTS
The Friday Harbor Laboratories and Department of Zoology of the University of Washington and
NSF grant OCE8400818 supported preparation of this summary.
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DATEACCEPTED: May 29, 1986.
ADDRESS: Friday Harbor Laboratories. 620 University Road. Friday Harbor, Wa ,hington 98250.