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The evolution of mating systems in tropical reef corals
PERSPECTIVES Potential mating systems in corals
The evolution of mating systems in tropical reef corals David B. Carlon The life histories of tropical reef corals (Scleractinia) include two traits that can strongly bias mating systems towards inbreeding: (1) most species express both sexes simultaneously, creating the potential for self-fertilization; and (2) there is philopatric dispersal of planktonic or demersal larvae. Recent studies have confirmed that all hermaphrodite species with broad dispersal potential are either completely, or almost completely, self-incompatible. By contrast, species with limited dispersal potential have high, but variable, rates of self-fertilization. This interspecific variation in coral mating systems is similar to that found in terrestrial plants. Understanding the selective forces that drive mating-system variation in marine environments will undoubtedly broaden our understanding of the evolution of inbreeding and outbreeding in sessile plants and animals. David Carlon is at the Wrigley Institute for Environmental Studies, University of Southern California, PO Box 5069, Avalon, CA 90704, USA ([email protected]).
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cornerstone of theoretical population biology is the assumption that any member of a population has an equal probability of mating with any other member of that population. Given random mating, patterns of genotypic diversity can be predicted from one generation to the next using the Hardy–Weinberg theorem. However, in the natural world random mating is one of a spectrum of possible mating systems that defines patterns of mating within populations. In sessile organisms, life-history variation plays a fundamental role in determining where a mating system will lie along this spectrum. For example, many terrestrial plants express both sexes either in the same flower or among flowers of the same plant leading to routine self-fertilization. At the other extreme, separate sexes and broadly dispersing spores, seeds or larvae virtually eliminate opportunities for inbreeding. Many marine invertebrates spawn gametes directly into the sea and fertilization success is largely determined by the physical characteristics (i.e. current speeds and distance between gamete sources) at the time of spawning1. Rapid dilution of gametes makes the success of fertilization proximity dependent, and this effect, coupled with larval dispersal in the order of hundreds and sometimes thousands of kilometers, will ensure random mating over very large spatial scales. Yet, an ecologically important proportion of benthic marine invertebrates possesses life-history traits that could lead to inbreeding at much smaller spatial scales2. These include the ascidians, barnacles, bryozoans, cnidarians TREE vol. 14, no. 12 December 1999
and sponges. Moreover, within these taxa there is often variation in life-history traits controlling larval dispersal. Such variation is likely to have dramatic consequences on patterns of syngamy within populations, yet mating systems are known for only a handful of populations3–6, and there is no systematic examination of mating-system variation within any of these ecologically important groups. The Anthozoa (sea anemones and corals) contain an extraordinary diversity of life-history variation at the species, population and individual levels. Consider reef-building corals that live in shallow tropical environments throughout the world’s oceans. In many species, both sexes are expressed within a single individual (simultaneous hermaphroditism), but in other species sexes are separate (gonochorism). Larval dispersal might also vary in a systematic fashion. Corals either brood larvae that are competent to settle upon release from the parent, or have planktonic larvae that require a week floating in surface waters to complete development. Coral populations could be inbred because of self-fertilization and/or limited dispersal, or largely outbred at the scale of hundreds of kilometers. Understanding the adaptive significance of mating-system variation is a fundamental problem in evolutionary biology and has a rich theoretical literature7. However, the framework of mating-system evolution, and particularly inbreeding, comes mainly from the study of terrestrial plants. Corals provide an opportunity to test and extend mating-system theory with a novel group of organisms that live in a completely different medium – the sea.
Like plants, corals are sessile, modular organisms that have demographic properties unique to clonal organisms8. The basic unit of all corals is the polyp, which is typically duplicated hundreds of times to form a colony. Although each polyp can theoretically act as a physiologically independent unit, reproductive characteristics such as the onset of maturity and timing of gametogenesis are synchronized at the colony level. More than two-thirds of the coral species studied express both sexes simultaneously, and in almost all cases male and female gametes are produced within each polyp9. Using botanical terminology, selfing in corals could occur in two ways: (1) by syngamy of gametes originating from a single polyp (autogamy); or (2) by syngamy of gametes from different polyps (geitonogamy). Within hermaphroditic corals, fertilization and development proceed along two distinct pathways. The most common pathway is broadcast spawning. In this mode, eggs and sperm are packaged together within gamete bundles that are either extruded slowly or forcibly ejected through the polyp mouth in synchronous, annual spawning events. These ‘mass spawning’ events can involve over 100 coral species (but dominated by Acropora and Montipora spp. corals) and numerous other invertebrates on the Great Barrier Reef of Australia10. After leaving the polyp mouth, the highly buoyant gamete bundles float to the surface where they break apart and fertilization occurs. Gamete packaging and synchronous spawning has two important consequences for patterns of mating. First, eggs and sperm from individual gamete bundles are their closest neighbors when they break up at the sea surface. Second, although gametes from different colonies will suffer stronger dilution effects, synchronicity within populations increases the abundance of outcross gametes at the time of syngamy. Although fewer species are involved, synchronous spawning phenomena have also been observed in the Caribbean Sea, the Red Sea, the Central Pacific, the Hawaiian Islands and Japan11,12. In addition to the spatial relations between selfed and outcrossed gametes, broadcasting development has important implications for dispersal potential of larvae. The resulting embryos require at least 4–7 days to complete development in the water column before they become competent to return to the benthos13. Consequently, the probability that any sibling or other relative settling near each other will be low. As the proximity of mates has strong effects on fertilization success in every marine organism
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PERSPECTIVES
Table 1. Numbers of tropical coral species with different life-history traits that influence inbreedinga Mode of larval developmentb Sexual expression
Brood
Broadcast
Hermaphroditic Gonochoric
17c,d 11d
115c 38
aAdapted
from Ref. 9. that brood larvae undergo internal fertilization and complete development within the parent. Corals that broadcast larvae undergo external fertilization and complete development while floating in the plankton. cSpecies have the potential for selfing. dSpecies have the potential for inbreeding through related outcrossing (biparental inbreeding). bCorals
studied so far, including corals1, it is highly unlikely that inbreeding by cross fertilization of related neighbors regularly occurs in broadcasting corals. Because inbreeding in plants and corals can occur from either selfing or through mating of relatives botanists have termed the latter biparental inbreeding. A second mode of development is less common at the species level, although it appears in some ecologically important species in the Caribbean Sea (e.g. Porites and Agaricia spp.) and other geographic areas. In brooding development, sperm are ejected in clouds, typically on a lunar cycle over several months. Fertilization occurs internally, and embryos develop within the parent for several weeks before release14. Newly released larvae are competent to metamorphose upon release from parents,
and behavior during dispersal suggests that some brooded larvae might attach within meters of adults15. Given that dispersal is more limited in brooding corals, outcrossing events are more likely to involve related individuals compared with species with broadcasting development. For example, philopatric dispersal and proximity-dependent fertilization success would make sibling–sibling, or parent–sibling mating more common compared with species with larvae that disperse beyond their natal reef. Of course the physical conditions when spawning occurs or larvae are released will play an important role in how far coral larvae will disperse16. The most common coral life history combines simultaneous hermaphroditism with broadcasting development; however, all four potential combinations
Box 1. Estimating mating-system parameters in simultaneous hermaphrodites At the population level, mating-system parameters have traditionally been estimated using either singlelocus, or multilocus mixed-mating models and allozyme data18. Single-locus models assume a fraction of progeny within populations that are selfed with probability s, and outcrossed t, with a probability of 1 2 s. Observed genotypes of several families (i.e. progeny arrays) are used to iteratively fit s and t to the model. Mixed-mating models assume that markers are neutral with respect to the control of the mating system, that the selfing rate is uniform across maternal parents, that no selection is occurring between syngamy and when progeny are sampled, and that the pollen (or sperm) pool is distributed uniformly across the population. Violation of this last assumption results in an upward bias of s, which makes single-locus models inappropriate for situations in which mating between relatives is expected (e.g. marine invertebrates with philopatric dispersal). Multilocus estimates of s are more robust to the effects of biparental inbreeding. The difference between s estimated by single-locus and multilocus models is a minimum estimate of the contribution of biparental inbreeding to the apparent selfing rate19. Multilocus models use data from several independent loci and the concept of detection probability to estimate t. Detection probability is the probability that outcross pollen or sperm contain a non-maternal allele averaged over all loci. As the detection probability approaches one, the outcross rate is simply the number of progeny with a non-maternal allele divided by the total number of progeny. Generally, 3–4 allozyme loci are needed to minimize variance associated with t when estimated with a multilocus model20. Detection probability is a function of both the number of loci and allelic diversity at each locus. The use of hyper-variable markers, such as microsatellite loci can provide high precision with only a few loci when allelic diversity is as high as ten alleles per locus. The traditional mating-system parameters s and t are components of female function and measure how many female zygotes are the result of selfing and outcrossing. Microsatellite markers should determine male fertility within individuals or populations because paternity of pollen or sperm can be assigned with high probability. Precise estimates of biparental inbreeding and heterogeneity of pollen or sperm pools at small spatial scales can be determined from multilocus microsatellite progeny arrays. As in almost every field of evolutionary biology, it is likely that new molecular tools will revolutionize how we think about the genetic components of matingsystem evolution.
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of sexual expression and developmental mode are represented in tropical environments (Table 1). Systematically, sexual expression tends to be conservative at the level of sub-order. For example, nearly all the Astrocoenia, which includes the extremely speciose family Acroporidae, are hermaphrodites. By comparison, the majority of Fungina are gonochores. There are some interesting exceptions to this general pattern. Within the family Favidae the ecologically dominant Montastraea annularis complex17 and M. cavernosa occur in similar habitats throughout the Caribbean Sea, yet species of the M. annularis complex are all hermaphrodites, whereas M. cavernosa has separate sexes. In contrast to the strong affinity of sexual expression with sub-orders and families, transitions between modes of development have occurred much more frequently within geographic regions. On the Great Barrier Reef and in the Central Pacific, species of Acropora might brood or broadcast, and in the Caribbean two Siderastrea spp. have contrasting developmental modes. The dominance of simultaneous hermaphroditism in corals creates opportunities for inbreeding through selfing in both broadcasting and brooding corals; however, mechanisms that permit this extreme form of inbreeding appear to have evolved only in those corals in which dispersal period is likely to be short.
Realized mating systems in corals Simultaneous hermaphroditism in broadcasting and brooding corals creates the potential for self-fertilization; however, the realized selfing rate is determined by both biochemical and morphological traits that limit or promote selfing, and ecological factors that control the availability of outcross gametes. There are two fundamental parameters of mating systems in which both sexes are expressed simultaneously. The first is the female selfing rate (s), which is the fraction of female embryos fertilized by selfing. It follows that the female outcrossing rate (t) = 1 2 s. With the appropriate genetic markers, s and t can be estimated within families or populations by comparing genotypes of maternal parents and progeny (Box 1). Obtaining parent progeny arrays to make these genotypic comparisons is simple in brooding invertebrates as matings that occur in the field are stored in larvae that develop within individual mothers, and larvae are readily released in laboratory cultures. The situation is more complicated in broadcasting corals where fertilization occurs at the water surface and the identity of neither parent is known. However, with highly variable markers TREE vol. 14, no. 12 December 1999
PERSPECTIVES the pool of potential adults can be characterized, and parentage assigned with reasonable probability21. In many broadcasting species estimating s and t from the field might be unnecessary because fertilization trials with 23 broadcasting species have revealed a low potential for selfing (Table 2). In these trials, male and female gametes from the same colony failed to produce viable embryos, or did so at very low rates. A notable exception is the high potential for selfing in Goniastrea favulus, which was later confirmed in controlled crosses between allogenic colonies in laboratory aquaria. In this experiment, more than half of each brood was the result of self-fertilization26. G. favulus has an unusual spawning behavior in which male and female gametes are ejected simultaneously in sticky mucous strings. Fertilization occurs within the mucous strings and negatively buoyant embryos sink to the reef surface to metamorphose near the parent colony. The result of this spawning behavior is extreme philopatry in larval recruitment, which has important consequences for the evolution of matingsystem parameters in sessile organisms. In brooding species, mating systems are only known for three species; however, the selfing rate in these species can be high. For example, I have used allozyme data of parents and progeny in Acropora palifera from the Great Barrier Reef27 to estimate the outcrossing rate using a single-locus, mixed-mating model. In this case, t = 0.246 with a confidence interval of 0.145. Considering that this apparently low outcrossing rate might be biased downward by biparental inbreeding (Box 1), it would be useful to know the population structure of this coral at small spatial scales. For example, limited gene flow within samples used for matingsystem analysis would suggest that biparental inbreeding is occurring. The population structure of A. palifera from One Tree Island of the Southern Great Barrier Reef28 is consistent with the effects of a high selfing rate, rather than biparental inbreeding. Samples from small isolated patch reefs located within 0.5 km had deficits of heterozygotes (positive Fis values), yet gene flow was high among these reefs (Fst values were not different from zero). If these allozyme loci are selectively neutral, the most parsimonious explanation for the high estimate of s and lack of heterozygosity in populations exchanging genes is that selfing dominates the mating system of A. palifera. More recently, individual selfing rates have been estimated using rapid amplified polymorphic DNA (RAPD) markers in two Caribbean brooders: Porites astreoides and Favia fragum6. Individual TREE vol. 14, no. 12 December 1999
Table 2. Self-compatibility in 23 hermaphroditic corals with broadcasting development Fertilization (%)a Family
Species
Self
Controls
Refs
Acroporidae
Acropora cytherea Acropora elseyi Acropora formosa Acropora hyacinthus Acropora longicyathus Acropora millepora Acropora pulchra Acropora selago Acropora tenuis Acropora valida Montipora digitata (FF) Montipora spumosa
8.0 4.0 0.5 0.6 1.0 1.2 5.2 0.0 0.5 13.0 0.0 0.0
96.0 93.0 99.0 95.0 92.0 49.0 56.0 94.0 98.0 93.0 45.0 30.0
22 22 22 22 22 22 22 22 22 22 22 22
Favidae
Goniastrea aspera Goniastrea favulus Platygyra daedalea Platygyra sp. H Platygyra lamellina Platygyra pini Platygyra ryukyuensis Platygyra sinensis Montastraea annularis b Montastraea faveolata b Montastraea franksi b
10.3 65.8 3.1 1.4 2.7 8.9 6.2 3.7 Low Variable Low
97.0 86.5 45.2 51.5 58.1 58.6 57.7 ND High High High
23 23 24 24 24 24 24 24 17,25 17,25 17,25
aPercentage of cleaving eggs (averaged across trials) with gametes from a single colony (self) or two different colonies (controls) presumed to be allogenic. bQualitative fertilization rates are reported for Montastrea trials as numbers of larvae were counted at the end of several days and the total number of eggs and/or sperm were not controlled.
selfing rates ranged from 0 to 0.79 in P. astreodies and 0.08 to 0.94 in F. fragum. However, confidence limits of these estimates were not calculated, apparently because of a lack of data on the frequency of informative bands in adult populations. Thus, for a handful of brooding species the potential for selfing is high, apparently much higher than broadcasting corals. Still, there is much work to be done with brooding species. Multilocus estimates of mating-system parameters combined with studies of small-scale genetic structure would allow the partitioning of the effects of selfing and biparental inbreeding on population structure. Additional insights into the effects of biparental inbreeding on population structure would come from studies of the gonochoric brooding corals as there is no selfing pathway to inbreeding in this life history. The pattern of nearly complete selfincompatibility in species with high dispersal potential (the majority of broadcasting species), yet high rates of selfing in the limited set of brooding species and G. favulus are striking. But why are broadcasting corals self-incompatible when there must be such strong selection on traits that minimize the dilution
of gametes at spawning, and why is apparently limited dispersal related to high selfing rates?
Mating-system theory for sessile organisms with variable dispersal The modern foundation of matingsystem theory is the inherent conflict between the genetic transmission advantage of selfing29 and the phenotypic costs of producing offspring that might suffer from inbreeding depression. Theoretically, outcrossed progeny must be twice as fit as selfed progeny for outcrossing to evolve30. This trade-off between the transmission advantage of selfing and the disadvantage of inbreeding depression makes two important assumptions. First, male gametes used for selfing must not reduce outcrossing success. This effect is known as ‘pollen discounting’ and can reduce the amount of pollen available for outcrossing, countering the genetic transmission advantage of selfing31. It is unclear if the equivalent of pollen discounting (i.e. sperm discounting) occurs in any marine invertebrate. The cost of sperm discounting will depend on the efficiency of selfed verses outcrossed fertilization and the ratio of sperm:egg production. In corals, the close proximity of
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PERSPECTIVES sperm and eggs within polyps of brooding parents, or gamete clusters in broadcasting species, should increase the fertilization efficiency of selfing relative to outcrossing, because outcross gametes must negotiate significantly larger spatial barriers to fertilization. If the allocation to male function compared with female function is high, which appears to be the case for several coral species32,33, then sperm required for selfing might represent a minimal cost to sperm available for outcrossing. More research is needed with marine invertebrates and corals to properly evaluate costs, if any, of sperm discounting in mating-system evolution. The second assumption that merits closer scrutiny is that outcrossed matings occur randomly with respect to the entire population. Biparental inbreeding has conflicting effects on the evolution of selfing34. On the one hand it can favor selfing by decreasing the difference in fitness between selfed and outcrossed progeny, and by reducing the genetic load within populations by the eventual purging of deleterious recessive alleles. On the other hand, increased biparental inbreeding decreases the genetic transmission advantage of selfing, because related parents involved in outcrossing are more likely to share copies of the same gene. Theoretically, models have shown that mixed mating systems (intermediate values of s) can be favored when biparental inbreeding is high35,36. Although there are no estimates of inbreeding depression in corals that can be used to test these models directly, we can predict inbreeding depression values given average larval dispersal distance and a fixed genetic load within populations. When larval dispersal is high, potential outcross mates are not expected to be related, and as a consequence the difference in fitness between selfed and outcrossed progeny should be large, favoring mating systems of outcrossing. Local dispersal in brooding species should increase biparental inbreeding, which will reduce inbreeding depression and favor either complete selfing or mixed mating systems. A positive relationship between dispersal and inbreeding depression can explain why widely dispersing corals, i.e. those with broadcasting development, have mating systems that are outbred, whereas potentially philopatric dispersal in brooding corals and the special case of G. favulus, have mating systems that are inbred.
organisms explicitly. As the spatial distribution and genetic identity of mates plays such an important role in patterns of syngamy in both terrestrial and marine environments, examination of population structure at small spatial scales, and its temporal variation, should yield a wealth of new insights into patterns of mating. The structure of coral populations at small and large scales are known for a few brooding species on the Great Barrier Reef28,37,38 and a broadcasting coral in Tawain39,but comparative studies between life-history variants conducted on the same spatial scale will be informative in relating dispersal to patterns of mating. Highly variable molecular markers will aid this cause, and allow precise estimates of biparental inbreeding. Dominant markers, such as RAPDs (Ref. 40), have already been applied to mating-system problems in corals6, but the development of codominant markers such as microsatellites for corals and other marine invertebrates will provide the fine-scale resolution necessary to define the genetic landscape of mating-system evolution. Although data are forthcoming in a few systems3,5, we know little of how inbreeding varies among populations and relates to lifehistory variation. Estimates of this effect are needed to test the theory but for many long-lived corals will be difficult to obtain. There are several fast growing and shorter lived corals (e.g. Pocillopora damicornis in the Pacific and F. fragum in the Atlantic) that would make suitable models for understanding the phenotypic consequences of different types of mating events. The potential for using marine systems for a deeper and more synthetic understanding of mating-system evolution clearly exists. Reaping this potential lies largely in documenting matingsystem variation among species and in different ecological conditions, and determining the evolutionary consequences of inbreeding and outbreeding in the sea.
Prospects
References
The rich life-history variation in tropical reef corals provides a system to test mating-system theory of sessile
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Acknowledgments I thank the students, postdoctoral researchers and faculty of the Center for Population Biology, University of California at Davis for valuable insights and discussion of mating-system evolution in sessile organisms. Suzanne Edmands and two anonymous reviewers made helpful comments on the manuscript. Spencer Barrett suggested this review was a good idea. I was supported by a Postdoctoral Fellowship in the Biosciences related to the Environment from the National Science Foundation while writing this perspective. 1 Levitan, D.R. and Petersen, C. (1995) Sperm limitation in the sea, Trends Ecol. Evol. 10, 228–231
2 Knowlton, N. and Jackson, J.B.C. (1993) Inbreeding and outbreeding in marine invertebrates, in Natural History of Inbreeding and Outbreeding (Thornhill, N.W., ed.), pp. 200–249, University of Chicago Press 3 Grosberg, R.K. (1987) Limited dispersal and proximity-dependent mating success in the colonial ascidian Botryllus schlosseri, Evolution 41, 372–384 4 Yund, P.O. and McCartney, M.A. (1994) Male reproductive success in sessile invertebrates: competition for fertilizations, Ecology 75, 2151–2167 5 Cohen, C.S. (1996) The effects of contrasting modes of fertilization on levels of inbreeding in the marine invertebrate genus Corella, Evolution 50, 1896–1907 6 Brazeau, D., Gleason, D.F. and Morgan, M.E. (1998) Self-fertilization in brooding hermaphroditic Caribbean corals: Evidence from molecular markers, J. Exp. Mar. Biol. Ecol. 231, 235–238 7 Uyenoyama, M.K., Holsinger, K.H. and Waller, D.M. (1993) Ecological and genetic factors directing the evolution of self-fertilization, in Oxford Surveys in Evolutionary Biology (Vol. 9) (Futuyma, D. and Antonovics, J., eds), pp. 327–382, Oxford University Press 8 Hughes, T.P., Ayre, D. and Connell, J.H. (1992) The evolutionary ecology of corals, Trends Ecol. Evol. 7, 292–295 9 Harrison, P.L. and Wallace, C.C. (1991) Reproduction, dispersal and recruitment of scleractinian corals, in Ecosystems of the World; Coral Reefs (Vol. 25) (Dubinsky, Z., ed.), pp. 133–207, Elsevier 10 Babcock, R.C. et al. (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef, Mar. Biol. 90, 379–394 11 Kinzie, R.A., III (1993) Spawning in the reef corals Pocillopora verrucosa and P. eydouxi at Sesoku Island, Okinawa, Galaxia 11, 93–105 12 Van Veghel, M.L.J. (1993) Multiple species spawning on Curacao Reefs, Bull. Mar. Sci. 52, 1017–1021 13 Babcock, R.C. and Heyward, A.J. (1986) Larval development of certain gamete-spawning scleractinian corals, Coral Reefs 5, 111–116 14 Szmant, A.M. (1986) Reproductive ecology of Caribbean reef corals, Coral Reefs 5, 43–54 15 Carlon, D.B. and Olson, R.R. (1993) Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals, J. Exp. Mar. Biol. Ecol. 173, 247–263 16 Willis, B.L. and Oliver, J.K. (1990) Direct tracking of coral larvae: implications for dispersal studies of planktonic larvae in topographically complex environments, Ophelia 31, 145–162 17 Knowlton, N. et al. (1997) Direct evidence for reproductive isolation among three species of the Montastraea annularis complex in Central America (Panama and Honduras), Mar. Biol. 127, 705–711 18 Brown, J., Burdon, J. and Jarosz, A.M. (1989) Isozyme analysis of plant mating systems, in Advances in Plant Sciences (Series 4) (Soltis, D.E. and Soltis, P.S., eds), pp. 73–86, Discorides Press 19 Schoen, D.J. and Clegg, M.T. (1984) Estimation of mating system parameters when outcrossing events are correlated, Proc. Natl. Acad. Sci. U. S. A. 81, 5258–5262 20 Ritland, K. and Jain, S. (1981) A model for the estimation of outcrossing rate and gene frequencies using n independent loci, Heredity 47, 35–52 TREE vol. 14, no. 12 December 1999
PERSPECTIVES 21 Coffroth, M.A. and Lasker, H.R. (1998) Larval paternity and male reproductive success of a broadcast-spawning gorgonian, Plexaura kuna, Mar. Biol. 131, 329–337 22 Willis, B.L. et al. (1997) Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning corals, Coral Reefs 16, S53–S65 23 Heyward, A.J. and Babcock, R.C. (1986) Selfand cross-fertilization in scleractinian corals, Mar. Biol. 90, 191–195 24 Miller, K.J. and Babcock, R.C. (1997) Conflicting morphological and reproductive species boundaries in the coral genus Platygrya, Biol. Bull. 192, 98–110 25 Szmant, A.M. et al. (1997) Hybridization within the species complex of scleractinian coral Montastraea annularis, Mar. Biol. 129, 561–572 26 Stoddart, J.A., Babcock, R.C. and Heyward, A.J. (1988) Self-fertilization and maternal enzymes in the planulae of the coral Goniastrea favulus, Mar. Biol. 99, 489–494 27 Ayre, D.J. and Resing, J.M. (1986) Sexual and asexual production of planlulae in reef corals, Mar. Biol. 90, 187–190 28 Benzie, J.A.H., Haskell, A. and Lehman, H. (1995) Variation in the genetic composition of coral (Pocillopora damicornis and Acropora
29 30
31
32
33
34
35
palifera) populations from different reef habitats, Mar. Biol. 121, 731–739 Fisher, R.A. (1941) Average excess and average effect of a gene substitution, Ann. Eugen. 11, 53–63 Lande, R. and Shemske, D.W. (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models, Evolution 39, 533–544 Harder, L.D. and Wilson, W.G. (1998) A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution, Am. Nat. 152, 684–695 Szmant-Foelich, A., Reutter, M. and Riggs, L. (1985) Sexual reproduction of Favia fragum (Esper): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico, Bull. Mar. Sci. 37, 880–892 Hall, V.R. and Hughes, T.P. (1996) Reproductive strategies of modular organisms – comparative studies of reef-building corals, Ecology 77, 950–963 Waller, D.M. (1993) The statics and dynamics of mating system evolution, in The Natural History of Inbreeding and Outbreeding (Thornhill, N., ed.), pp. 97–117, University of Chicago Press Uyenoyama, M.K. (1986) Inbreeding and the cost of meiosis: the evolution of selfing in
The modern synthesis, Ronald Fisher and creationism The ‘modern evolutionary synthesis’ convinced most biologists that natural selection was the only directive influence on adaptive evolution. Today, however, dissatisfaction with the synthesis is widespread, and creationists and antidarwinians are multiplying. The central problem with the synthesis is its failure to show (or to provide distinct signs) that natural selection of random mutations could account for observed levels of adaptation. Egbert Leigh, Jr is at the Smithsonian Tropical Research Institute, Smithsonian Institution, Washington, DC 20560-0580, USA.
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synthesis untestable8, sterile9,10 and outmoded11: creationists and antidarwinians (Box 1) are as numerous and as vocal as ever.
Making natural selection a deus ex machina
Egbert Giles Leigh, Jr
he modern evolutionary synthesis1 is founded upon the proposition that natural selection is the directive influence on adaptive evolution. This synthesis was established by combining deductive reasoning with the elimination of competing hypotheses by empirical research. Work of systematists2 and geneticists3,4, on the stages of speciation, confirmed Darwin’s view that speciation rarely involves discontinuous ‘saltations’ (polyploidy being the principal exception). Geneticists3–5 falsified neo-Lamarckism and mutation-driven theories of evolution; and paleontologists6 revealed
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populations practicing partial biparental inbreeding, Evolution 40, 388–404 Uyenoyama, M.K. and Antonovics, J. (1987) The evolutionary dynamics of mixed mating systems: on the adaptive value of selfing and biparental inbreeding, in Perpectives in Ethology, Vol. 7: Alternatives (Bateson, P.P.G. and Klopfer, H., eds), pp. 125–152, Plenum Press Ayre, D.J. and Dufty, S. (1994) Evidence for restricted gene flow in the viviporous coral Seriatophora hystrix on Australia’s Great Barrier Reef, Evolution 48, 1183–1201 Ayre, D.J., Hughes, T.P. and Standish, R.J. (1997) Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia, Mar. Ecol. Prog. Ser. 59, 175–187 Yu, J.K. et al. (1999) Genetic structure of a scleractinian coral, Mycedium elephantotus, in Tawain, Mar. Biol. 133, 21–28 Grosberg, R.K., Levitan, D.R. and Cameron, B.B. (1996) Characterization of genetic structure and genealogies using RAPD-PCR markers: a random primer for the novice and nervous, in Molecular Zoology: Advances, Strategies, and Protocols (Ferraris, J.D. and Palumbi, S.R., eds), pp. 67–100, Wiley Liss
the environmental, opportunity-driven context of evolution, applying the ‘coup de grace’ to theories of mutation-driven orthogenesis. Eliminating these pseudoexplanations seemed to lift a thick fog from the subject. Mayr7 remarked, ‘No one who has not witnessed it himself can imagine the confusion and dissension that characterized the pre-Synthesis period.’ The three classics2,4,6 that established the American version of the synthesis overflow with a sense of triumph and hope: finally there was a reliable basis for understanding evolution. However, biologists have since declared the
The primary problem with the synthesis is that its makers established natural selection as the director of adaptive evolution by eliminating competing explanations7, not by providing evidence that natural selection among ‘random’ mutations could, or did, account for observed adaptation (Box 2). Mayr12 remarked, ‘As these non-Darwinian explanations were refuted during the synthesis … natural selection automatically became the universal explanation of evolutionary change (together with chance factors).’ Depriving the synthesis of plausible alternatives, which seemed such a triumph, in fact sowed the seeds of its faults. Direct demonstration of the relationships between available variation, natural selection and evolution was neglected for several reasons. First, the task seemed formidable13. The physicist Polkinghorne observed: ‘Someone like Richard Dawkins can present persuasive pictures of how the sifting and accumulation of small differences can produce large-scale developments, but, instinctively, a physical scientist would like to see an estimate, however rough, of how many small steps
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The evolution of mating systems in tropical reef corals David B. Carlon The life histories of tropical reef corals (Scleractinia) include two traits that can strongly bias mating systems towards inbreeding: (1) most species express both sexes simultaneously, creating the potential for self-fertilization; and (2) there is philopatric dispersal of planktonic or demersal larvae. Recent studies have confirmed that all hermaphrodite species with broad dispersal potential are either completely, or almost completely, self-incompatible. By contrast, species with limited dispersal potential have high, but variable, rates of self-fertilization. This interspecific variation in coral mating systems is similar to that found in terrestrial plants. Understanding the selective forces that drive mating-system variation in marine environments will undoubtedly broaden our understanding of the evolution of inbreeding and outbreeding in sessile plants and animals. David Carlon is at the Wrigley Institute for Environmental Studies, University of Southern California, PO Box 5069, Avalon, CA 90704, USA ([email protected]).
A
cornerstone of theoretical population biology is the assumption that any member of a population has an equal probability of mating with any other member of that population. Given random mating, patterns of genotypic diversity can be predicted from one generation to the next using the Hardy–Weinberg theorem. However, in the natural world random mating is one of a spectrum of possible mating systems that defines patterns of mating within populations. In sessile organisms, life-history variation plays a fundamental role in determining where a mating system will lie along this spectrum. For example, many terrestrial plants express both sexes either in the same flower or among flowers of the same plant leading to routine self-fertilization. At the other extreme, separate sexes and broadly dispersing spores, seeds or larvae virtually eliminate opportunities for inbreeding. Many marine invertebrates spawn gametes directly into the sea and fertilization success is largely determined by the physical characteristics (i.e. current speeds and distance between gamete sources) at the time of spawning1. Rapid dilution of gametes makes the success of fertilization proximity dependent, and this effect, coupled with larval dispersal in the order of hundreds and sometimes thousands of kilometers, will ensure random mating over very large spatial scales. Yet, an ecologically important proportion of benthic marine invertebrates possesses life-history traits that could lead to inbreeding at much smaller spatial scales2. These include the ascidians, barnacles, bryozoans, cnidarians TREE vol. 14, no. 12 December 1999
and sponges. Moreover, within these taxa there is often variation in life-history traits controlling larval dispersal. Such variation is likely to have dramatic consequences on patterns of syngamy within populations, yet mating systems are known for only a handful of populations3–6, and there is no systematic examination of mating-system variation within any of these ecologically important groups. The Anthozoa (sea anemones and corals) contain an extraordinary diversity of life-history variation at the species, population and individual levels. Consider reef-building corals that live in shallow tropical environments throughout the world’s oceans. In many species, both sexes are expressed within a single individual (simultaneous hermaphroditism), but in other species sexes are separate (gonochorism). Larval dispersal might also vary in a systematic fashion. Corals either brood larvae that are competent to settle upon release from the parent, or have planktonic larvae that require a week floating in surface waters to complete development. Coral populations could be inbred because of self-fertilization and/or limited dispersal, or largely outbred at the scale of hundreds of kilometers. Understanding the adaptive significance of mating-system variation is a fundamental problem in evolutionary biology and has a rich theoretical literature7. However, the framework of mating-system evolution, and particularly inbreeding, comes mainly from the study of terrestrial plants. Corals provide an opportunity to test and extend mating-system theory with a novel group of organisms that live in a completely different medium – the sea.
Like plants, corals are sessile, modular organisms that have demographic properties unique to clonal organisms8. The basic unit of all corals is the polyp, which is typically duplicated hundreds of times to form a colony. Although each polyp can theoretically act as a physiologically independent unit, reproductive characteristics such as the onset of maturity and timing of gametogenesis are synchronized at the colony level. More than two-thirds of the coral species studied express both sexes simultaneously, and in almost all cases male and female gametes are produced within each polyp9. Using botanical terminology, selfing in corals could occur in two ways: (1) by syngamy of gametes originating from a single polyp (autogamy); or (2) by syngamy of gametes from different polyps (geitonogamy). Within hermaphroditic corals, fertilization and development proceed along two distinct pathways. The most common pathway is broadcast spawning. In this mode, eggs and sperm are packaged together within gamete bundles that are either extruded slowly or forcibly ejected through the polyp mouth in synchronous, annual spawning events. These ‘mass spawning’ events can involve over 100 coral species (but dominated by Acropora and Montipora spp. corals) and numerous other invertebrates on the Great Barrier Reef of Australia10. After leaving the polyp mouth, the highly buoyant gamete bundles float to the surface where they break apart and fertilization occurs. Gamete packaging and synchronous spawning has two important consequences for patterns of mating. First, eggs and sperm from individual gamete bundles are their closest neighbors when they break up at the sea surface. Second, although gametes from different colonies will suffer stronger dilution effects, synchronicity within populations increases the abundance of outcross gametes at the time of syngamy. Although fewer species are involved, synchronous spawning phenomena have also been observed in the Caribbean Sea, the Red Sea, the Central Pacific, the Hawaiian Islands and Japan11,12. In addition to the spatial relations between selfed and outcrossed gametes, broadcasting development has important implications for dispersal potential of larvae. The resulting embryos require at least 4–7 days to complete development in the water column before they become competent to return to the benthos13. Consequently, the probability that any sibling or other relative settling near each other will be low. As the proximity of mates has strong effects on fertilization success in every marine organism
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PERSPECTIVES
Table 1. Numbers of tropical coral species with different life-history traits that influence inbreedinga Mode of larval developmentb Sexual expression
Brood
Broadcast
Hermaphroditic Gonochoric
17c,d 11d
115c 38
aAdapted
from Ref. 9. that brood larvae undergo internal fertilization and complete development within the parent. Corals that broadcast larvae undergo external fertilization and complete development while floating in the plankton. cSpecies have the potential for selfing. dSpecies have the potential for inbreeding through related outcrossing (biparental inbreeding). bCorals
studied so far, including corals1, it is highly unlikely that inbreeding by cross fertilization of related neighbors regularly occurs in broadcasting corals. Because inbreeding in plants and corals can occur from either selfing or through mating of relatives botanists have termed the latter biparental inbreeding. A second mode of development is less common at the species level, although it appears in some ecologically important species in the Caribbean Sea (e.g. Porites and Agaricia spp.) and other geographic areas. In brooding development, sperm are ejected in clouds, typically on a lunar cycle over several months. Fertilization occurs internally, and embryos develop within the parent for several weeks before release14. Newly released larvae are competent to metamorphose upon release from parents,
and behavior during dispersal suggests that some brooded larvae might attach within meters of adults15. Given that dispersal is more limited in brooding corals, outcrossing events are more likely to involve related individuals compared with species with broadcasting development. For example, philopatric dispersal and proximity-dependent fertilization success would make sibling–sibling, or parent–sibling mating more common compared with species with larvae that disperse beyond their natal reef. Of course the physical conditions when spawning occurs or larvae are released will play an important role in how far coral larvae will disperse16. The most common coral life history combines simultaneous hermaphroditism with broadcasting development; however, all four potential combinations
Box 1. Estimating mating-system parameters in simultaneous hermaphrodites At the population level, mating-system parameters have traditionally been estimated using either singlelocus, or multilocus mixed-mating models and allozyme data18. Single-locus models assume a fraction of progeny within populations that are selfed with probability s, and outcrossed t, with a probability of 1 2 s. Observed genotypes of several families (i.e. progeny arrays) are used to iteratively fit s and t to the model. Mixed-mating models assume that markers are neutral with respect to the control of the mating system, that the selfing rate is uniform across maternal parents, that no selection is occurring between syngamy and when progeny are sampled, and that the pollen (or sperm) pool is distributed uniformly across the population. Violation of this last assumption results in an upward bias of s, which makes single-locus models inappropriate for situations in which mating between relatives is expected (e.g. marine invertebrates with philopatric dispersal). Multilocus estimates of s are more robust to the effects of biparental inbreeding. The difference between s estimated by single-locus and multilocus models is a minimum estimate of the contribution of biparental inbreeding to the apparent selfing rate19. Multilocus models use data from several independent loci and the concept of detection probability to estimate t. Detection probability is the probability that outcross pollen or sperm contain a non-maternal allele averaged over all loci. As the detection probability approaches one, the outcross rate is simply the number of progeny with a non-maternal allele divided by the total number of progeny. Generally, 3–4 allozyme loci are needed to minimize variance associated with t when estimated with a multilocus model20. Detection probability is a function of both the number of loci and allelic diversity at each locus. The use of hyper-variable markers, such as microsatellite loci can provide high precision with only a few loci when allelic diversity is as high as ten alleles per locus. The traditional mating-system parameters s and t are components of female function and measure how many female zygotes are the result of selfing and outcrossing. Microsatellite markers should determine male fertility within individuals or populations because paternity of pollen or sperm can be assigned with high probability. Precise estimates of biparental inbreeding and heterogeneity of pollen or sperm pools at small spatial scales can be determined from multilocus microsatellite progeny arrays. As in almost every field of evolutionary biology, it is likely that new molecular tools will revolutionize how we think about the genetic components of matingsystem evolution.
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of sexual expression and developmental mode are represented in tropical environments (Table 1). Systematically, sexual expression tends to be conservative at the level of sub-order. For example, nearly all the Astrocoenia, which includes the extremely speciose family Acroporidae, are hermaphrodites. By comparison, the majority of Fungina are gonochores. There are some interesting exceptions to this general pattern. Within the family Favidae the ecologically dominant Montastraea annularis complex17 and M. cavernosa occur in similar habitats throughout the Caribbean Sea, yet species of the M. annularis complex are all hermaphrodites, whereas M. cavernosa has separate sexes. In contrast to the strong affinity of sexual expression with sub-orders and families, transitions between modes of development have occurred much more frequently within geographic regions. On the Great Barrier Reef and in the Central Pacific, species of Acropora might brood or broadcast, and in the Caribbean two Siderastrea spp. have contrasting developmental modes. The dominance of simultaneous hermaphroditism in corals creates opportunities for inbreeding through selfing in both broadcasting and brooding corals; however, mechanisms that permit this extreme form of inbreeding appear to have evolved only in those corals in which dispersal period is likely to be short.
Realized mating systems in corals Simultaneous hermaphroditism in broadcasting and brooding corals creates the potential for self-fertilization; however, the realized selfing rate is determined by both biochemical and morphological traits that limit or promote selfing, and ecological factors that control the availability of outcross gametes. There are two fundamental parameters of mating systems in which both sexes are expressed simultaneously. The first is the female selfing rate (s), which is the fraction of female embryos fertilized by selfing. It follows that the female outcrossing rate (t) = 1 2 s. With the appropriate genetic markers, s and t can be estimated within families or populations by comparing genotypes of maternal parents and progeny (Box 1). Obtaining parent progeny arrays to make these genotypic comparisons is simple in brooding invertebrates as matings that occur in the field are stored in larvae that develop within individual mothers, and larvae are readily released in laboratory cultures. The situation is more complicated in broadcasting corals where fertilization occurs at the water surface and the identity of neither parent is known. However, with highly variable markers TREE vol. 14, no. 12 December 1999
PERSPECTIVES the pool of potential adults can be characterized, and parentage assigned with reasonable probability21. In many broadcasting species estimating s and t from the field might be unnecessary because fertilization trials with 23 broadcasting species have revealed a low potential for selfing (Table 2). In these trials, male and female gametes from the same colony failed to produce viable embryos, or did so at very low rates. A notable exception is the high potential for selfing in Goniastrea favulus, which was later confirmed in controlled crosses between allogenic colonies in laboratory aquaria. In this experiment, more than half of each brood was the result of self-fertilization26. G. favulus has an unusual spawning behavior in which male and female gametes are ejected simultaneously in sticky mucous strings. Fertilization occurs within the mucous strings and negatively buoyant embryos sink to the reef surface to metamorphose near the parent colony. The result of this spawning behavior is extreme philopatry in larval recruitment, which has important consequences for the evolution of matingsystem parameters in sessile organisms. In brooding species, mating systems are only known for three species; however, the selfing rate in these species can be high. For example, I have used allozyme data of parents and progeny in Acropora palifera from the Great Barrier Reef27 to estimate the outcrossing rate using a single-locus, mixed-mating model. In this case, t = 0.246 with a confidence interval of 0.145. Considering that this apparently low outcrossing rate might be biased downward by biparental inbreeding (Box 1), it would be useful to know the population structure of this coral at small spatial scales. For example, limited gene flow within samples used for matingsystem analysis would suggest that biparental inbreeding is occurring. The population structure of A. palifera from One Tree Island of the Southern Great Barrier Reef28 is consistent with the effects of a high selfing rate, rather than biparental inbreeding. Samples from small isolated patch reefs located within 0.5 km had deficits of heterozygotes (positive Fis values), yet gene flow was high among these reefs (Fst values were not different from zero). If these allozyme loci are selectively neutral, the most parsimonious explanation for the high estimate of s and lack of heterozygosity in populations exchanging genes is that selfing dominates the mating system of A. palifera. More recently, individual selfing rates have been estimated using rapid amplified polymorphic DNA (RAPD) markers in two Caribbean brooders: Porites astreoides and Favia fragum6. Individual TREE vol. 14, no. 12 December 1999
Table 2. Self-compatibility in 23 hermaphroditic corals with broadcasting development Fertilization (%)a Family
Species
Self
Controls
Refs
Acroporidae
Acropora cytherea Acropora elseyi Acropora formosa Acropora hyacinthus Acropora longicyathus Acropora millepora Acropora pulchra Acropora selago Acropora tenuis Acropora valida Montipora digitata (FF) Montipora spumosa
8.0 4.0 0.5 0.6 1.0 1.2 5.2 0.0 0.5 13.0 0.0 0.0
96.0 93.0 99.0 95.0 92.0 49.0 56.0 94.0 98.0 93.0 45.0 30.0
22 22 22 22 22 22 22 22 22 22 22 22
Favidae
Goniastrea aspera Goniastrea favulus Platygyra daedalea Platygyra sp. H Platygyra lamellina Platygyra pini Platygyra ryukyuensis Platygyra sinensis Montastraea annularis b Montastraea faveolata b Montastraea franksi b
10.3 65.8 3.1 1.4 2.7 8.9 6.2 3.7 Low Variable Low
97.0 86.5 45.2 51.5 58.1 58.6 57.7 ND High High High
23 23 24 24 24 24 24 24 17,25 17,25 17,25
aPercentage of cleaving eggs (averaged across trials) with gametes from a single colony (self) or two different colonies (controls) presumed to be allogenic. bQualitative fertilization rates are reported for Montastrea trials as numbers of larvae were counted at the end of several days and the total number of eggs and/or sperm were not controlled.
selfing rates ranged from 0 to 0.79 in P. astreodies and 0.08 to 0.94 in F. fragum. However, confidence limits of these estimates were not calculated, apparently because of a lack of data on the frequency of informative bands in adult populations. Thus, for a handful of brooding species the potential for selfing is high, apparently much higher than broadcasting corals. Still, there is much work to be done with brooding species. Multilocus estimates of mating-system parameters combined with studies of small-scale genetic structure would allow the partitioning of the effects of selfing and biparental inbreeding on population structure. Additional insights into the effects of biparental inbreeding on population structure would come from studies of the gonochoric brooding corals as there is no selfing pathway to inbreeding in this life history. The pattern of nearly complete selfincompatibility in species with high dispersal potential (the majority of broadcasting species), yet high rates of selfing in the limited set of brooding species and G. favulus are striking. But why are broadcasting corals self-incompatible when there must be such strong selection on traits that minimize the dilution
of gametes at spawning, and why is apparently limited dispersal related to high selfing rates?
Mating-system theory for sessile organisms with variable dispersal The modern foundation of matingsystem theory is the inherent conflict between the genetic transmission advantage of selfing29 and the phenotypic costs of producing offspring that might suffer from inbreeding depression. Theoretically, outcrossed progeny must be twice as fit as selfed progeny for outcrossing to evolve30. This trade-off between the transmission advantage of selfing and the disadvantage of inbreeding depression makes two important assumptions. First, male gametes used for selfing must not reduce outcrossing success. This effect is known as ‘pollen discounting’ and can reduce the amount of pollen available for outcrossing, countering the genetic transmission advantage of selfing31. It is unclear if the equivalent of pollen discounting (i.e. sperm discounting) occurs in any marine invertebrate. The cost of sperm discounting will depend on the efficiency of selfed verses outcrossed fertilization and the ratio of sperm:egg production. In corals, the close proximity of
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PERSPECTIVES sperm and eggs within polyps of brooding parents, or gamete clusters in broadcasting species, should increase the fertilization efficiency of selfing relative to outcrossing, because outcross gametes must negotiate significantly larger spatial barriers to fertilization. If the allocation to male function compared with female function is high, which appears to be the case for several coral species32,33, then sperm required for selfing might represent a minimal cost to sperm available for outcrossing. More research is needed with marine invertebrates and corals to properly evaluate costs, if any, of sperm discounting in mating-system evolution. The second assumption that merits closer scrutiny is that outcrossed matings occur randomly with respect to the entire population. Biparental inbreeding has conflicting effects on the evolution of selfing34. On the one hand it can favor selfing by decreasing the difference in fitness between selfed and outcrossed progeny, and by reducing the genetic load within populations by the eventual purging of deleterious recessive alleles. On the other hand, increased biparental inbreeding decreases the genetic transmission advantage of selfing, because related parents involved in outcrossing are more likely to share copies of the same gene. Theoretically, models have shown that mixed mating systems (intermediate values of s) can be favored when biparental inbreeding is high35,36. Although there are no estimates of inbreeding depression in corals that can be used to test these models directly, we can predict inbreeding depression values given average larval dispersal distance and a fixed genetic load within populations. When larval dispersal is high, potential outcross mates are not expected to be related, and as a consequence the difference in fitness between selfed and outcrossed progeny should be large, favoring mating systems of outcrossing. Local dispersal in brooding species should increase biparental inbreeding, which will reduce inbreeding depression and favor either complete selfing or mixed mating systems. A positive relationship between dispersal and inbreeding depression can explain why widely dispersing corals, i.e. those with broadcasting development, have mating systems that are outbred, whereas potentially philopatric dispersal in brooding corals and the special case of G. favulus, have mating systems that are inbred.
organisms explicitly. As the spatial distribution and genetic identity of mates plays such an important role in patterns of syngamy in both terrestrial and marine environments, examination of population structure at small spatial scales, and its temporal variation, should yield a wealth of new insights into patterns of mating. The structure of coral populations at small and large scales are known for a few brooding species on the Great Barrier Reef28,37,38 and a broadcasting coral in Tawain39,but comparative studies between life-history variants conducted on the same spatial scale will be informative in relating dispersal to patterns of mating. Highly variable molecular markers will aid this cause, and allow precise estimates of biparental inbreeding. Dominant markers, such as RAPDs (Ref. 40), have already been applied to mating-system problems in corals6, but the development of codominant markers such as microsatellites for corals and other marine invertebrates will provide the fine-scale resolution necessary to define the genetic landscape of mating-system evolution. Although data are forthcoming in a few systems3,5, we know little of how inbreeding varies among populations and relates to lifehistory variation. Estimates of this effect are needed to test the theory but for many long-lived corals will be difficult to obtain. There are several fast growing and shorter lived corals (e.g. Pocillopora damicornis in the Pacific and F. fragum in the Atlantic) that would make suitable models for understanding the phenotypic consequences of different types of mating events. The potential for using marine systems for a deeper and more synthetic understanding of mating-system evolution clearly exists. Reaping this potential lies largely in documenting matingsystem variation among species and in different ecological conditions, and determining the evolutionary consequences of inbreeding and outbreeding in the sea.
Prospects
References
The rich life-history variation in tropical reef corals provides a system to test mating-system theory of sessile
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Acknowledgments I thank the students, postdoctoral researchers and faculty of the Center for Population Biology, University of California at Davis for valuable insights and discussion of mating-system evolution in sessile organisms. Suzanne Edmands and two anonymous reviewers made helpful comments on the manuscript. Spencer Barrett suggested this review was a good idea. I was supported by a Postdoctoral Fellowship in the Biosciences related to the Environment from the National Science Foundation while writing this perspective. 1 Levitan, D.R. and Petersen, C. (1995) Sperm limitation in the sea, Trends Ecol. Evol. 10, 228–231
2 Knowlton, N. and Jackson, J.B.C. (1993) Inbreeding and outbreeding in marine invertebrates, in Natural History of Inbreeding and Outbreeding (Thornhill, N.W., ed.), pp. 200–249, University of Chicago Press 3 Grosberg, R.K. (1987) Limited dispersal and proximity-dependent mating success in the colonial ascidian Botryllus schlosseri, Evolution 41, 372–384 4 Yund, P.O. and McCartney, M.A. (1994) Male reproductive success in sessile invertebrates: competition for fertilizations, Ecology 75, 2151–2167 5 Cohen, C.S. (1996) The effects of contrasting modes of fertilization on levels of inbreeding in the marine invertebrate genus Corella, Evolution 50, 1896–1907 6 Brazeau, D., Gleason, D.F. and Morgan, M.E. (1998) Self-fertilization in brooding hermaphroditic Caribbean corals: Evidence from molecular markers, J. Exp. Mar. Biol. Ecol. 231, 235–238 7 Uyenoyama, M.K., Holsinger, K.H. and Waller, D.M. (1993) Ecological and genetic factors directing the evolution of self-fertilization, in Oxford Surveys in Evolutionary Biology (Vol. 9) (Futuyma, D. and Antonovics, J., eds), pp. 327–382, Oxford University Press 8 Hughes, T.P., Ayre, D. and Connell, J.H. (1992) The evolutionary ecology of corals, Trends Ecol. Evol. 7, 292–295 9 Harrison, P.L. and Wallace, C.C. (1991) Reproduction, dispersal and recruitment of scleractinian corals, in Ecosystems of the World; Coral Reefs (Vol. 25) (Dubinsky, Z., ed.), pp. 133–207, Elsevier 10 Babcock, R.C. et al. (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef, Mar. Biol. 90, 379–394 11 Kinzie, R.A., III (1993) Spawning in the reef corals Pocillopora verrucosa and P. eydouxi at Sesoku Island, Okinawa, Galaxia 11, 93–105 12 Van Veghel, M.L.J. (1993) Multiple species spawning on Curacao Reefs, Bull. Mar. Sci. 52, 1017–1021 13 Babcock, R.C. and Heyward, A.J. (1986) Larval development of certain gamete-spawning scleractinian corals, Coral Reefs 5, 111–116 14 Szmant, A.M. (1986) Reproductive ecology of Caribbean reef corals, Coral Reefs 5, 43–54 15 Carlon, D.B. and Olson, R.R. (1993) Larval dispersal distance as an explanation for adult spatial pattern in two Caribbean reef corals, J. Exp. Mar. Biol. Ecol. 173, 247–263 16 Willis, B.L. and Oliver, J.K. (1990) Direct tracking of coral larvae: implications for dispersal studies of planktonic larvae in topographically complex environments, Ophelia 31, 145–162 17 Knowlton, N. et al. (1997) Direct evidence for reproductive isolation among three species of the Montastraea annularis complex in Central America (Panama and Honduras), Mar. Biol. 127, 705–711 18 Brown, J., Burdon, J. and Jarosz, A.M. (1989) Isozyme analysis of plant mating systems, in Advances in Plant Sciences (Series 4) (Soltis, D.E. and Soltis, P.S., eds), pp. 73–86, Discorides Press 19 Schoen, D.J. and Clegg, M.T. (1984) Estimation of mating system parameters when outcrossing events are correlated, Proc. Natl. Acad. Sci. U. S. A. 81, 5258–5262 20 Ritland, K. and Jain, S. (1981) A model for the estimation of outcrossing rate and gene frequencies using n independent loci, Heredity 47, 35–52 TREE vol. 14, no. 12 December 1999
PERSPECTIVES 21 Coffroth, M.A. and Lasker, H.R. (1998) Larval paternity and male reproductive success of a broadcast-spawning gorgonian, Plexaura kuna, Mar. Biol. 131, 329–337 22 Willis, B.L. et al. (1997) Experimental hybridization and breeding incompatibilities within the mating systems of mass spawning corals, Coral Reefs 16, S53–S65 23 Heyward, A.J. and Babcock, R.C. (1986) Selfand cross-fertilization in scleractinian corals, Mar. Biol. 90, 191–195 24 Miller, K.J. and Babcock, R.C. (1997) Conflicting morphological and reproductive species boundaries in the coral genus Platygrya, Biol. Bull. 192, 98–110 25 Szmant, A.M. et al. (1997) Hybridization within the species complex of scleractinian coral Montastraea annularis, Mar. Biol. 129, 561–572 26 Stoddart, J.A., Babcock, R.C. and Heyward, A.J. (1988) Self-fertilization and maternal enzymes in the planulae of the coral Goniastrea favulus, Mar. Biol. 99, 489–494 27 Ayre, D.J. and Resing, J.M. (1986) Sexual and asexual production of planlulae in reef corals, Mar. Biol. 90, 187–190 28 Benzie, J.A.H., Haskell, A. and Lehman, H. (1995) Variation in the genetic composition of coral (Pocillopora damicornis and Acropora
29 30
31
32
33
34
35
palifera) populations from different reef habitats, Mar. Biol. 121, 731–739 Fisher, R.A. (1941) Average excess and average effect of a gene substitution, Ann. Eugen. 11, 53–63 Lande, R. and Shemske, D.W. (1985) The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models, Evolution 39, 533–544 Harder, L.D. and Wilson, W.G. (1998) A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution, Am. Nat. 152, 684–695 Szmant-Foelich, A., Reutter, M. and Riggs, L. (1985) Sexual reproduction of Favia fragum (Esper): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico, Bull. Mar. Sci. 37, 880–892 Hall, V.R. and Hughes, T.P. (1996) Reproductive strategies of modular organisms – comparative studies of reef-building corals, Ecology 77, 950–963 Waller, D.M. (1993) The statics and dynamics of mating system evolution, in The Natural History of Inbreeding and Outbreeding (Thornhill, N., ed.), pp. 97–117, University of Chicago Press Uyenoyama, M.K. (1986) Inbreeding and the cost of meiosis: the evolution of selfing in
The modern synthesis, Ronald Fisher and creationism The ‘modern evolutionary synthesis’ convinced most biologists that natural selection was the only directive influence on adaptive evolution. Today, however, dissatisfaction with the synthesis is widespread, and creationists and antidarwinians are multiplying. The central problem with the synthesis is its failure to show (or to provide distinct signs) that natural selection of random mutations could account for observed levels of adaptation. Egbert Leigh, Jr is at the Smithsonian Tropical Research Institute, Smithsonian Institution, Washington, DC 20560-0580, USA.
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synthesis untestable8, sterile9,10 and outmoded11: creationists and antidarwinians (Box 1) are as numerous and as vocal as ever.
Making natural selection a deus ex machina
Egbert Giles Leigh, Jr
he modern evolutionary synthesis1 is founded upon the proposition that natural selection is the directive influence on adaptive evolution. This synthesis was established by combining deductive reasoning with the elimination of competing hypotheses by empirical research. Work of systematists2 and geneticists3,4, on the stages of speciation, confirmed Darwin’s view that speciation rarely involves discontinuous ‘saltations’ (polyploidy being the principal exception). Geneticists3–5 falsified neo-Lamarckism and mutation-driven theories of evolution; and paleontologists6 revealed
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populations practicing partial biparental inbreeding, Evolution 40, 388–404 Uyenoyama, M.K. and Antonovics, J. (1987) The evolutionary dynamics of mixed mating systems: on the adaptive value of selfing and biparental inbreeding, in Perpectives in Ethology, Vol. 7: Alternatives (Bateson, P.P.G. and Klopfer, H., eds), pp. 125–152, Plenum Press Ayre, D.J. and Dufty, S. (1994) Evidence for restricted gene flow in the viviporous coral Seriatophora hystrix on Australia’s Great Barrier Reef, Evolution 48, 1183–1201 Ayre, D.J., Hughes, T.P. and Standish, R.J. (1997) Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia, Mar. Ecol. Prog. Ser. 59, 175–187 Yu, J.K. et al. (1999) Genetic structure of a scleractinian coral, Mycedium elephantotus, in Tawain, Mar. Biol. 133, 21–28 Grosberg, R.K., Levitan, D.R. and Cameron, B.B. (1996) Characterization of genetic structure and genealogies using RAPD-PCR markers: a random primer for the novice and nervous, in Molecular Zoology: Advances, Strategies, and Protocols (Ferraris, J.D. and Palumbi, S.R., eds), pp. 67–100, Wiley Liss
the environmental, opportunity-driven context of evolution, applying the ‘coup de grace’ to theories of mutation-driven orthogenesis. Eliminating these pseudoexplanations seemed to lift a thick fog from the subject. Mayr7 remarked, ‘No one who has not witnessed it himself can imagine the confusion and dissension that characterized the pre-Synthesis period.’ The three classics2,4,6 that established the American version of the synthesis overflow with a sense of triumph and hope: finally there was a reliable basis for understanding evolution. However, biologists have since declared the
The primary problem with the synthesis is that its makers established natural selection as the director of adaptive evolution by eliminating competing explanations7, not by providing evidence that natural selection among ‘random’ mutations could, or did, account for observed adaptation (Box 2). Mayr12 remarked, ‘As these non-Darwinian explanations were refuted during the synthesis … natural selection automatically became the universal explanation of evolutionary change (together with chance factors).’ Depriving the synthesis of plausible alternatives, which seemed such a triumph, in fact sowed the seeds of its faults. Direct demonstration of the relationships between available variation, natural selection and evolution was neglected for several reasons. First, the task seemed formidable13. The physicist Polkinghorne observed: ‘Someone like Richard Dawkins can present persuasive pictures of how the sifting and accumulation of small differences can produce large-scale developments, but, instinctively, a physical scientist would like to see an estimate, however rough, of how many small steps
Published by Elsevier Science Ltd. PII: S0169-5347(99)01725-5
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