Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
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, 616 STRATHMANN: SUMMARY STATEMENT ON EVOLUTION 617 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 618 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 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: SUMMARY STATEMENT ON EVOLUTION 619 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- 620 BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 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. LITERATURE CITED Burton, R. S. and M. W. Feldman. 1982. Population genetics of coastal and estuarine invertebrates; does larval behavior influence population structure? Pages 537-551 in V. S. Kennedy, ed. Estuarine comparisons. Academic Press, New York. Caswell, H. 1981. The evolution of "mixed" life histories in marine invertebrates and elsewhere. Am. Nat. 117: 529-536. Chaffee, C. and R. R. Strathmann. 1984. Constraints on egg masses. I. Retarded development within thick egg masses. J. Exp. Mar. BioI. Ecol. 84: 73-84. Charlesworth, D. and B. Charlesworth. 1981. Allocation of resources to male and female functions in hermaphrodites. BioI. J. Linn. Soc. 14: 57-74. Charnov, E. L. 1982. The theory of sex allocation. Princeton University Press, Princeton, New Jersey. 355 pp. Christiansen, F. B. and T. M. Fenchel. 1979. Evolution of marine invertebrate reproductive patterns. Theor. Popul. BioI. 16: 267-282. Grahame, J. 1982. Energy flow and breeding in two species of Lacuna: comparative costs of egg production and maintenance. Int. J. Invertebr. Reprod. 5: 91-99. Grant, A. 1983. On the evolution of brood protection in marine benthic invertebrates. Am. Nat. 122: 549-555. Hansen, T. A. 1980. Influence of larval dispersal and geographic distribution on species longevity in neogastropods. Paleobiology 6: 193-207. Highsmith, R. C. 1985. Floating and algal rafting as potential dispersal mechanisms in brooding invertebrates. Mar. Ecol. Prog. Ser. 25: 169-179. Hughes, R. N. and D. J. Roberts. 1980. Reproductive effort of winkles (Littorina spp.) with contrasted methods of reproduction. Oecologia 47: 130-136. Jablonski, D. and R. A. Lutz. 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. BioI. Rev. 58: 21-89. MacKay, T. F. C. and R. W. Doyle. 1978. An ecological genetic analysis of the settling behaviour of a marine polychaete: 1. Probability of settlement and gregarious behaviour. Heredity 40: 1-12. 622 BULLETIN OFMARINESCIENCE, VOL.39, NO.2, 1986 Palmer, A. R. and R. R. Strathmann. 1981. Scale of dispersal in varying environments and its implications for life histories of marine invertebrates. Oecologia 48: 308-318. Pechenik, J. A. 1979. Role of encapsulation in invertebrate life histories. Am. Nat. 114: 859-870. Scheltema, R. S. 1977. Dispersal of marine invertebrate organisms: paleobiogeographic and biostratigraphic implications. Pages 73-108 in E. G. Kauffman and J. E. Hazel, eds. Concepts and methods in biostratigraphy. Dowden, Hutchinson, and Ross, Stroudsburg, Pennsylvania. Schroeder, P. C. and C. O. Hermans. 1975. Annelida: Polychaeta. Pages 1-213 in A. C. Giese and J. S. Pearse, eds. Reproduction of marine invertebrates, Vol. 3, Annelids and Echiurans. Academic Press, New York. Shuto, T. 1974. Larval ecology of prosobranch gastropods and its bearing on biogeography and paleontology. Lethaia 7: 239-256. Strathmann, R. R. 1974. The spread of sibling larvae of sedentary marine invertebrates. Am. Nat. 108: 29-44. ---. 1977. Egg size, larval development, and juvenile size in benthic marine invertebrates. Am. Nat. III: 373-376. ---. 1978a. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32: 894-906. ---. 1978b. Progressive vacating of adaptive types during the Phanerozoic. Evolution 32: 907914. ---. 1982. Selection for retention or export oflarvae in estuaries. Pages 521-536 in V. S. Kennedy, ed. Estuarine comparisons. Academic Press, New York. ---. 1985. Feeding and nonfeeding larval development and life-history evolution in marine invertebrates. Ann. Rev. Ecol. Syst. 16: 339-361. --. 1986. Larval feeding. Chapter 7 in A. C. Giese and J. S. Pearse, eds. Reproduction of marine invertebrates, Vol. 9. Blackwell Press. --and C. Chaffee. 1984. Constraints on egg masses. 2. Effect of spacing, size, and number of eggs on ventilation of masses of embryos in jelly, adherent groups, or thin walled capsules. J. Exp. Mar. BioI. Ecol. 84: 85-93. --and M. F. Strathmann. 1982. The relation between adult size and brooding in marine invertebrates. Am. Nat. 119: 91-101. ---, --and R. H. Emson. 1984. Does limited brood capacity link adult size, brooding, and simultaneous hermaphroditism? A test with the starfish Asterina phylactica. Am. Nat. 123: 796818. Thorson, G. 1950. Reproductive and larval ecology of marine invertebrat~s. Bi.ll Rev. 25: 1-45. Todd, C. D. and R. W. Doyle. 1981. Reproductive strategies of marine benthic invertebrates: a settlement timing hypothesis. Mar. Ecol. Prog. Ser. 4: 75-83. Vance, R. R. 1973. On reproductive strategies in marine benthic invertebrues. Am. Nat. 107: 339352. DATEACCEPTED: May 29, 1986. ADDRESS: Friday Harbor Laboratories. 620 University Road. Friday Harbor, Wa ,hington 98250.