Models of reticulate evolution in the coral genus Acropora based on chromosome numbers: parallels with plants.
One well-documented mechanism for rapid speciation in plants is hybridization. Veron (1995) has suggested that corals are like plants, and indeed they share a number of attributes. Asexual propagation through fragmentation or fission is an important reproductive strategy demonstrated both by plants (Stebbins 1950; Grant 1981; Silander 1985) and corals (Hughes and Cancino 1985; Jackson 1985; Jackson and Hughes 1985; Hughes et al. 1992). Similar complexities of sexual reproductive strategies (Veron 1995), the potential heritability of somatic mutations (Buss 1985; Fautin, in press), and other parallels (Knowlton and Jackson 1993) have increasingly stimulated coral biologists to look to terrestrial plants as instructive analogs. Polyploidy is also an important mechanism of speciation in the plant kingdom (Stebbins 1950; Goldblatt 1980; Lewis 1980b), but is thought to be rare in animals. Might polyploidy be a cytogenetic mechanism that has also operated in the diversification of Acropora?
Chromosomal studies can provide important evidence for past hybridization events. Two previous studies (Wijsman and Wijsman-Best 1973; Heyward 1985) have attempted to examine scleractinian coral chromosomes, but neither included members of the genus Acropora. In this paper, I present chromosome counts for 22 species of Acropora, using mitotic cells of externally developing embryos. Chromosome numbers were also established for three species of Montipora and one Fungia species. A model that applies established principles of plant cytogenetics is presented to account for the observed interspecific differences in coral chromosome number.
MATERIALS AND METHODS
Corals were obtained from Guam (Pago Bay), Okinawa (Sesoko Island), Australia (Magnetic Island), Palau, and Hawaii (Kaneohe Bay, Oahu). Species were identified by reference to field guides (Wallace 1978; Randall and Myers 1983; Veron 1986; Nishihira 1988; Uchida and Fukuda 1989), comparison with museum specimens (University of Guam Marine Laboratory, Mangilao; Bishop Museum, Honolulu; Museum of Tropical Queensland, Townsville), and personal communication with taxonomic experts (R. Randall; C. Wallace). Voucher specimens of corals from Guam, Okinawa, and Palau were deposited in the collections of the Bishop Museum in Honolulu. Voucher specimens of corals from Australia were deposited in the collections of the Museum of Tropical Queensland in Townsville.
Acropora and Montipora are simultaneous hermaphrodites, and spawning consists of the release of eggs and sperm, which have been packaged together into discrete bundles, from the mouths of fertile polyps (Babcock and Heyward 1986). The primary method of controlling gamete encounter involved placing several conspecific colonies together in a separate aquarium with no water flow when egg/sperm bundles were seen protruding from the polyp mouth, and allowing them to spawn. Seawater for aquaria in which spawning corals were placed was collected early in the day, prior to spawning in the field, to avoid introducing foreign sperm into the aquaria. Thirty to 60 minutes after spawning ceased, eggs were collected with a wide-mouth pipette and transferred to a culture container filled with 0.45 [Mu]m Millipore-filtered seawater (MFS).
Presence of colored eggs in fertile colonies (Harrison et al. 1984; Babcock et al. 1986; Heyward et al. 1987) and records of previous spawning events in Guam (Richmond and Hunter 1990; Kenyon 1994), Okinawa (Heyward et al. 1987), Australia (Harrison et al. 1984; Willis et al. 1985; Babcock et al. 1986), Hawaii (Hunter 1988; Cox 1991; D. Krupp, pers. comm. 1992), and Palau (Kenyon 1995) were used to predict spawning dates. Ripe colonies or viable portions of colonies were maintained for several days before a predicted spawning date in flow-through aquaria.
Corallites of the solitary gonochoric coral Fungia scutaria were isolated in individual finger bowls several hours before predicted spawning times. The negatively buoyant eggs from several colonies were pipetted into a culture container filled with MFS, and several drops of seawater into which a male colony had spawned were added from each of several male colonies.
Embryonic development was facilitated by mild agitation such as that provided by a roller apparatus or incubation of capped containers in a mesh bag attached to a buoyed line on the reef. Embryos were treated with colchicine, followed by a hypotonic solution to spread the chromosomes, and then a fixative for preservation. Various combinations of treatment parameters were tried to optimize results. The ranges of manipulated variables were: (1) age of embryo: 4.75-12 h; (2) concentration of colchicine-seawater: 0.02% or 0.05% (w/v); (3) duration of treatment with colchicine: 30-180 min; (4) concentration of hypotonic solution: 80:20, 70:30, or 65:35 seawater:tapwater; and (5) duration of treatment with hypotonic solution: 15-30 min. Treated embryos were fixed in three changes of freshly mixed, absolute ethanol:50% glacial acetic acid (1:1, v/v) and refrigerated during storage.
To remove lipids prior to staining, fixed embryos were soaked in diethyl ether for 4-6 h, then briefly returned to fixative. Embryos were stained with 2% lacto-aceto-orcein on a glass slide for 15 min, gently rinsed with tapwater, and squashed under a cover slip. Dehydration of squash preparations was retarded for several days by sealing the cover slip edges with clear nail polish.
Squashes were scanned for cells in which the chromosome complement was clearly distinct from that of other cells and the chromosomes were well spread. Chromosomes were counted in each of 45 metaphase spreads for each species, with the exception of A. gemmifera embryos, for which only 25 useful metaphase spreads could be found. For each spread, a lower and an upper limit for the number of chromosomes present was recorded, and a frequency distribution was constructed (Rahat et al. 1985).
The most useful chromosome preparations were those in which embryos 10-11 h old were cultured with colchicine for 2 h, followed by a 65:35 seawater:tapwater hypotonic treatment. The two different colchicine concentrations did not result in visible differences in chromosome appearance. Lengthy treatment of mitotic tissue with colchicine can induce polyploidy (Dewey 1980), as chromosomes replicate but do not move to opposite poles in the absence of a mitotic spindle. In some embryos of some species subjected to colchicine treatment times of 180 min, indications of induced polyploidy could be seen. This consisted of a few cells with a large number of very small chromosomes. The small size of the chromosomes, the infrequency of such duplicated complements, and comparison with cultures treated for shorter periods of time made it easy to distinguish cells in which polyploidy had been induced by the prolonged colchicine treatment.
The number of embryos that were examined for each species varied from 16 (M. verrucosa) to 114 (A. formosa). Considerable inter- and intraspecific variation in the degree of chromatin condensation made it difficult to establish reliable, comparative chromosome morphologies. In all species in which complements with compact, rod-shaped chromosomes were found, chromosomes ranged from 1-5 [Mu]m in length.
Most metaphase spreads had some degree of chromosome overlap, such that each individual chromosome could not always be uniquely resolved and counted. Additionally, the hypotonic solution that spreads the chromosomes may cause an artificial loss or gain of some chromosomes from an adjacent complement (Rahat et al. 1985). Consequently, a range of chromosome counts was obtained for all species [ILLUSTRATION FOR FIGURES 1, 2 OMITTED]. For each species, however, the modal number in the frequency distribution of metaphase spread chromosome counts was readily evident, and was chosen as representing the number of chromosomes for that species (Rahat et al. 1985). There was no association, for any of the species studied, between variation from the modal number of chromosomes and individual embryos from which counts were obtained.
Somatic chromosome numbers in Acropora ranged from 24 to 54 [ILLUSTRATION FOR FIGURE 1 OMITTED]. Sixteen species had 28 chromosomes. Chromosome numbers of 24, 30, 30, 42, 48, and 54 were established for the six other species.
Fungia scutaria, M. verrucosa, M. spumosa, and M. digitata all had 28 chromosomes [ILLUSTRATION FOR FIGURE 2 OMITTED]. Unlike eggs of Acropora and Fungia, Montipora eggs contain zooxanthellae when they are spawned (Krupp 1983; Babcock and Heyward 1986). Zooxanthellae in Montipora embryos did not appear disrupted by the colchicine and hypotonic treatments, and did not obscure clear views of coral chromosome complements.
The somatic chromosome number of 28 established here for 16 species of Acropora, three species of Montipora, and one species of Fungia is the same as that reported by Heyward (1985) for three other species of scleractinian coral (Goniopora lobata, Lobophyllia hemprichii, and Montipora dilitata). The disparate somatic numbers of 24, 30, 42, 48 and 54 found for six species of Acropora may have arisen through the combined processes of polyploidy and aneuploidy.
Polyploidy is a chromosomal alteration in which an organism possesses more than two complete chromosome sets. For example, in the angiosperm genus Festuca there are species in which the somatic 2n = 14 (diploid), 28 (tetraploid), 42 (hexaploid), 56 (octopioid), and 70 (decaploid), where n represents the number of chromosomes in the gametes. These somatic numbers are based on the gametic chromosome number of the diploid species, which is known as the basic chromosome number (x). In a diploid species n = x, but in a polyploid species n is a multiple of x.
Two extreme categories of polyploidy can be recognized: autopolyploidy and allopolyploidy. Autopolyploids derive replicate chromosome sets from a single parent species. Allopolyploids arise through hybridization between two chromosomally differentiated taxa (Stebbins 1950; White 1973, 1978; Stace 1980; Grant 1981). A hybrid is usually sterile, but may be able to propagate itself asexually (Grant and Grant 1992). Fertility can be restored to the hybrid by mitotic nondisjunction in the germ cell line, allowing the production of gametes through normal meiosis. When two such gametes combine, the result is a viable, fertile organism with a chromosome number that is the combined somatic number of its parents. Polyploids may arise from parents with either the same or different chromosome number.
Three primary conditions are conducive to the development of allopolyploidy: (1) the ability to form viable interspecific hybrids; (2) the ability to reproduce asexually, so that a hybrid might propagate, and the rare events of non-disjunction might have increased chances of occurring; and (3) the production of unreduced gametes. Among perennial angiosperms (Dawson 1962; Stebbins 1950, 1970; White 1973, 1978; Grant 1981), ferns (Wagner and Wagner 1980), mosses (Crosby 1980), and protists (Godward 1966; Nichols 1980; Stebbins and Hill 1980; Clayton 1988), polyploidy is especially prevalent in those species with effective means of vegetative reproduction. The spatial replication and temporal longevity of clonemate genomes increases the opportunities for the rare cytogenetic events that are necessary for polyploidy to arise. Polyploid complexes, the result of continued polyploidization in different anastomosing lineages, have been described for many plant genera (Stebbins 1950; White 1978; Grant 1981). In sexually reproducing plant populations, the union of unreduced gametes is one of the most important mechanisms by which polyploid individuals arise (Lewis 1980c; Grant 1981). The high incidence of polyploid angiosperms and ferns in glaciated regions of northern Europe has been interpreted as an effect of species from different refugia quickly moving into the land that was newly made available for colonization after the retreat of Pleistocene ice sheets (Stebbins 1950, 1970; Dawson 1962).
Many of these phenomena and conditions are likely to characterize corals in the genus Acropora. Experimental hybrids between species form and survive readily (Richmond 1992; Willis et al. 1992; Kenyon 1994; Wallace and Willis 1994), and mass spawning on a single night (Babcock et al. 1986; Heyward et al. 1987; Dai et al. 1992; Kenyon 1994) provides many opportunities for gametes of different species to interact. Acroporids, particularly the branching species, are well known for their tendency to propagate almost exclusively by fragmentation (Bak and Engel 1979; Tunnicliffe 1981; Highsmith 1982; Rylaarsdam 1983; Hughes 1985; Wallace 1985). The coexistence of several overlapping generations (Potts and Garthwaite 1991; Hughes et al. 1992) can facilitate development of a polyploid complex by enhancing the possibility of contact between gametes of different ploidy levels produced in different generations.
Finally, somatic mutations are potentially heritable in cnidarians (Campbell 1974; Buss 1985; Hughes 1989; Hughes et al. 1992), including those in which cells become polyploid through a dysfunctional mitotic spindle. Such mutations are known to be common in animals (White 1973; Brodsky and Uryvaeva 1985) and could be an important source of unreduced gametes. Despite its geological record back to the early Tertiary, Acropora does not seem to acquire its modern ecological prominence until several million years ago during the Plio-Pleistocene (Geister 1992). Rapid, sympatric speciation by polyploidy may have been facilitated in Acropora by the availability of new shallow-water habitats during sea-level transgressions, as well as by changing patterns of ocean circulation producing different patterns of geographical affinities among populations (Veron 1995).
Several mechanisms of aneuploid decrease or increase are well documented in angiosperm evolution, including descending and ascending dysploidy, nullisomy, and tetrasomy (Stebbins 1950; Darlington 1973; White 1978; Stace 1980; Grant 1981). Increases or decreases in the gametic chromosome number that occur on the diploid level are known as dysploidy. Descending dysploidy reduces the basic chromosome number, x. Sequential descending dysploidy results in several basic numbers (e.g., x = 8, 7, and 6) being represented within a related taxonomic group. In contrast, ascending dysploidy increases the gametic chromosome number. A given taxon may demonstrate both descending and ascending dysploidy. For example, the original basic number in the angiosperm genus Clarkia (Onagraceae) is x = 7 (Lewis 1953), but descendent basic numbers of x = 6 and x = 5, as well as ascendent basic numbers of x = 8 and x = 9, are also found. Polyploidy can subsequently become superimposed upon several basic numbers that have been generated by dysploidy. In the plant genus Carex (Cyperaceae) there are polyploid series derived from each of the basic numbers x = 5, 6, 7, 8, and 9, as well as polyploids derived from hybridization between lineages with different basic numbers (Stebbins 1950; Grant 1981). Nullisomy (the loss of a chromosome pair) and tetrasomy (the duplication of a chromosome pair) can further alter the number of chromosomes in a polyploid series (Darlington 1973; Stace 1980; Grant 1981).
Models of Somatic Chromosome Number Variation
The inference of a basic number in a polyploid series is an important step in fitting chromosome numbers to an evolutionary hypothesis. In the species studied to date, a somatic chromosome number of 28 was found in corals belonging to four families placed in three suborders according to traditional morphological criteria (Wells 1956), or in two clades that diverged more than 240 M.Y.B.P. according to a phylogeny constructed from analysis of mitochondrial DNA (Romano and Palumbi 1996). These facts suggest that the basic scleractinian chromosome number x = 14. In a polyploid model based on this assumption [ILLUSTRATION FOR FIGURE 3 OMITTED], 28 somatic chromosomes represents a diploid condition. Thirty somatic chromosomes originate through tetrasomy, while a tetraploid with 56 somatic chromosomes is reduced by nullisomy to 54 somatic chromosomes. A second basic number x = 12 is generated through descending dysploidy; 24 and 48 somatic chromosomes represent diploid and tetraploid derivatives, respectively. Forty-two somatic chromosomes, exemplified by A. valida, represents a triploid condition originating through backcrossing between tetraploid and diploid forms. Triploids generally have low fertility due to the production of unbalanced gametes during meiosis; in contrast, experimental intraspecific crosses with A. valida demonstrated high levels of fertilization success, comparable to those of experimental intraspecific crosses with other species (Kenyon 1994). However, the cytogenetic mechanisms of gamete production and egg activation have yet to be determined in scleractinian corals. Gynogenesis, the activation of unreduced eggs by sperm, may account for high fertility levels, as is known in triploid populations of several teleost fish species (Schultz 1980; Boron 1992).
An alternative possibility is that the basic scleractinian chromosome number is x = 7, and that 28 somatic chromosomes represents a tetraploid number (2n = 4x = 28), a hypothesis analogous to a common situation in plants. Many genera and some families of woody angiosperms have high apparent basic numbers in the range x = 12 to x = 21. Some authors regard these not as true basic numbers but as old polyploids from an earlier cycle of evolution (Stebbins 1950, 1970; Darlington 1973; Grant 1981), an idea supported by isozyme and DNA data (Soltis and Soltis 1990; Soltis et al. 1992). Several authors have suggested that the original basic number of the angiosperms lies in the range x = 7-9 (Ehrendorfer 1964; White 1978; Grant 1981), and recent fossil evidence supports this idea (Masterson 1994). Sometimes the diploid members of a series have disappeared from a genus or even a family, erasing evidence of the lower numbers (Stebbins 1950; Darlington 1973; White 1978; Grant 1981).
An alternative model of reticulate evolution [ILLUSTRATION FOR FIGURE 4 OMITTED] proposes that the scleractinian basic number x = 7 characterized a pool of ancestral diploids, 2n = 2x = 14. Independent events of tetraploidy may have anciently occurred in separate clades, as delineated by mitochondrial DNA criteria (Romano and Palumbi 1996), or more recently in multiple family lineages, giving rise to distantly related species bearing the same tetraploid somatic chromosome number of 28. From such an ancestral acroporid tetraploid derivative (2n = 4x = 28) many other Acropora species have radiated since the Eocene (Potts 1984, 1985; Rosen 1984; McManus 1985). Relative to the original basic number x = 7, the chromosome number 42 represents hexaploidy, generated by chromosome doubling in a triploid, in turn produced by the backcrossing of tetraploid and diploid forms. The chromosome number 54 is nullisomic, generated through loss of a pair of chromosomes from an octopioid (8x - 2). Through descending dysploidy, a second basic number x = 6 was derived, relative to which the somatic chromosome numbers 24 and 48 are tetraploids and octoploids, respectively. A third basic number x = 8 was derived from x = 7 through ascending dysploidy, from which ancestral diploids 2n = 2x = 16 were generated. Hybridization at the diploid level between ancestral types with 14 and 16 somatic chromosomes generated sterile hybrids with 15 somatic chromosomes; chromosome doubling then converted the hybrids to dibasic allotetraploids with 30 somatic chromosomes.
Parallel models can be found in the angiosperm genera Vicia and Claytonia. In the genus Vicia, somatic chromosome numbers of 10, 12, 14, 24, and 28 consist of diploids and tetraploids derived from two basic numbers (x = 6 and 7), accompanied by aneuploidy (Stace 1980). The polyploid complex in the North American genus Claytonia (Portulacaceae) is structured around three basic numbers (x = 6, 7, and 8), each of which has given rise to separate polyploid lineages, interlineage polyploids, and aneuploids clustering around the ploidy levels (White 1973; Grant 1981).
The latter model [ILLUSTRATION FOR FIGURE 4 OMITTED] is consistent with ploidy levels attained by angiosperms over an evolutionary time scale comparable to that of the family Acroporidae. Angiosperms radiated in the early Cretaceous, about 130 M.Y.B.P.. Most angiosperm polyploid lineages have not proceeded beyond the octopioid level (Stebbins 1950; White 1978; Grant 1981). Many of the 16 extant families of scleractinian corals first appear in the fossil record during the Cretaceous, with the family Acroporidae appearing about 100 M.Y.B.P. (Wells 1956; Veron 1986). The genus Acropora emerged during the Eocene, about 60 M.Y.B.P. (Wells 1956), but the ages of living species are not known (Potts 1985). Octopioid levels of cytogenetic development within the Acropora are therefore plausible within the time scales involved. The diploid taxa with 14 somatic chromosomes from which tetraploids emerged may have become extinct, or may still exist but have not yet been found.
Determination of DNA content in somatic cells of acroporids hypothesized to represent different ploidy levels would be useful in supporting or opposing the polyploid concept suggested by chromosome numbers, as successive ploidy levels should be accompanied by stepwise increases in nuclear DNA content (Schultz 1980). No genome size data are yet available for corals (McMillan and Miller 1989; McMillan et al. 1991). Veron and Wallace (1984) arranged the 70 species within the subgenus Acropora (Acropora), which occur off eastern Australia, into 14 'species groups' based on morphological similarity, to which A. ocellata, which is not found in east Australian waters, was later added (Veron 1990, 1993). The phylogenetic validity of these groups is unknown. The addition of somatic chromosome number to species arranged in their groups (Table 1) raises two discrepancies between the models presented here and the groups of Veron and Wallace (1984). According to the models, A. ocellata is more closely related to A. danai than to other members of the A. humilis group. According to the latter model [ILLUSTRATION FOR FIGURE 4 OMITTED], A. gemmifera and A. divaricata are more closely related to each other than to corals with 28 somatic chromosomes or to any of the other acroporids for which somatic chromosome number has been determined. Data derived from hybridization of cloned repeated sequences of DNA that are present throughout the subgenus Acropora but not present in other genera in the family Acroporidae (McMillan and Miller 1990), as well as nucleotide sequencing in this highly repeated base-pair sequence (McMillan et al. 1991) also imply different intrageneric relationships than those based on morphological criteria. The application of these molecular techniques would be useful in testing the relationships outlined in the models presented here. Of the results generated to date using molecular criteria (McMillan et al. 1988, 1991; McMillan and Miller 1988, 1989, 1990), none are contrary to relationships proposed by the models based on somatic chromosome numbers. While the former model [ILLUSTRATION FOR FIGURE 3 OMITTED] is more parsimonious, the assumptions in both models regarding basic scleractinian coral chromosome number are themselves hypotheses that can be tested in part by further chromosome counts in additional genera and families, as somatic chromosome number has been established for fewer than 5% of Indo-West Pacific scleractinian corals.
TABLE 1. Chromosome number by morphologically similar groups. Species of Acropora for which chromosome number has been determined are arranged according to "species groups" of Veron and Wallace (1984). Number of chromosomes is shown in parentheses. A. humilis group A. aspera group A. nasuta group A. gemmifera (30) A. pulchra (28) A. valida (42) A. monticulosa (28) A. millepora (28) A. lutkeni (28) A. samoensis (28) A. digitifera (28) A. selago group A. echinata group A. ocellata (48) A. tenuis (28) A. carduus (28) A. robusta group A. hyacinthus group A. elseyi (54) A. robusta (28) A. cytherea (28) A. Ioripes group A. danai (24) A. hyacinthus (28) A. loripes (28) A. nobilis (28) (= A. surculosa)(*) (= A. squarrosa)(*) A. formosa group A. divaricata group A. florida group A. formosa (28) A. clathrata (28) A. florida (28) A. divaricata (30) * Synonymized by Veron and Wallace (1984).
I thank R. Richmond for making available the facilities of the University of Guam Marine Lab, and K. Yamazato for extending the invitation to work at Sesoko Marine Science Center in Okinawa. B. Willis and C. Wallace generously shared their expertise and facilities at Magnetic Island, Australia. As representative of The Nature Conservancy, C. Cook expedited work in Palau, as did N. Idechong, Chief of Marine Resources of the Republic of Palau. F. Te and P. Chirichetti assisted with collections in Guam. For sharing coral gametes on spawning nights, I additionally thank D. Krupp, E. Cox, F. Stanton, F. Rivera, P. Harrison, R. Babcock, B. Stobart, and R. Rowan. R. Kinzie, J. Stimson, R. Richmond, S. Haley, G. Carr, R. Kowal, N. Knowlton, and an anonymous reviewer gave useful comments on the manuscript. Research was supported by the Lerner-Gray Fund of the American Museum of Natural History and, at the University of Hawaii at Manoa, by the Charles and Margaret Edmondson Fund, the International Agreements Fund of the School of Hawaiian, Asian, and Pacific Studies, and Research Corporation of the University of Hawaii.
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|Author:||Kenyon, Jean C.|
|Date:||Jun 1, 1997|
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