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AMER. ZOOL., 39:131-145 (1999) Genetic Structure of Coral Reef Organisms: Ghosts of Dispersal Past1 JOHN A. H. BENZIE 2 Australian Institute of Marine Science, PMB No 3., Townsville MC, Queensland 4810, Australia SYNOPSIS. Molecular genetic studies are revealing the presence of cryptic taxa, and patterns of gene flow in coral reef species, that do not correspond to present day ocean circulation patterns. Concordant borders of genetic inhomogeneity in several taxa emphasise the influence of historical barriers to gene flow. The persistence of genetic differences between sites apparently connected by present-day currents provides evidence for lack of effective contemporary gene exchange. A review of the limited data available to date cannot be conclusive, but suggests that present patterns of genetic variation in the Indo-Pacific have resulted from highly pulsed dispersal events associated with range expansion during interglacial periods. Thus, population genetic structure appears to be dominated by events associated with global climate change and sea level fluctuation during the last 1-3 million years, rather than vicariant geological events in the early Caenozoic. Regional speciation outside the tropical Indo-West Pacific and movement of these species into that region may have played a more important role in producing diversity in that region than traditionally recognised. Some genetic variants have arisen before, and have persisted through, several cycles of climate change. The genetic structure of populations is likely to have been maintained for several thousand years after they were first established, during or immediately after range expansion, by the occurrence of co-adapted gene complexes of some form, and because of more limited opportunity for dispersal than has been assumed to date. pattern and timing of gene flow. This inAn instructive approach to understanding formation can provide considerable insight how coral reef species and communities into the evolutionary history of species or might respond to global change is to ex- species complexes (Avise, 1994; Cunningamine how they have been affected by ham and Collins, 1994). For example, mochanges in the past. Information from fossil lecular data have proved useful in testing material, and data on the genetic structure hypotheses of the origin and age of northof present-day populations, provide pow- ern floras and faunas that invaded sites folerful and complementary means of detect- lowing the disappearance of the ice sheets ing and interpreting past influences on the (Hewitt, 1993, 1996). This information has earth's biota. Veron (1995), Potts (1999), provided a rich source from which to interand Pandolfi (1999) review the palaeonto- pret the effects of climate change, inferred logical data for coral reefs. This paper will independently from fossil pollen and inconcentrate on interpreting the results of sects, and from geological data. The data molecular analysis of population structure available for coral reef species are more limited, but there is sufficient information and phylogeny of coral reef species. Spatial patterns of variation in the fre- to allow a preliminary synthesis and interquencies of molecular variants, and the ex- pretation of the effects of past global clitent of the divergence between these vari- mate change. ants, can be used to determine the nature, INTRODUCTION REVIEW OF AVAILABLE DATA 1 From the Symposium Coral Reefs and Environmental Changes—Adaptation, Acclimation, or Extinction presented at the annual Meeting of the Society for Comparative and Integrative Biology, January 3-7, 1998, at Boston Massachusetts. 2 E-mail: [email protected] Three main sources of data are available: the genetic structure of tropical marine species, the molecular phylogeny and estimates of the times of divergence of coral reef species, and biogeographical interpretations of 131 132 JOHN A. H. BENZIE the patterns of distribution of molecular variants and tropical coral reef biotas. The genetic structure of tropical marine species Although early genetic studies on a few species provided evidence consistent with high dispersal among widespread marine species (Campbell et al, 1975; Winans, 1980), recent taxonomic and genetic work suggests that dispersal may be far more limited, and regional differentiation far stronger, than previously thought (Knowlton, 1993; Benzie, 1998). Sharp and congruent genetic discontinuities in several marine species have been detected on the Florida coast where there are no obvious barriers to dispersal (Avise, 1994). Many cryptic species are being discovered in what were considered single widespread taxa (Knowlton, 1993). Some of these {e.g., the Leptasterias starfish complex in the USA [Foltz et al, 1996]) appear to form a series of regionally differentiated taxa whose ranges abut each other, while others {e.g., Montastrea [Knowlton, 1993]) are sympatric. Information on tropical or coral reef species is limited, but Benzie (1998) has reviewed the data which exist for giant clams, Tridacna spp., sea urchins Echinometra spp., butterflyfish Chaetodon spp., the coconut crab Birgus latro, pearl oysters Pinctada margaritifera, and the starfish, Linckia laevigata and Acanthaster planci. Significant genetic differentiation has been detected among populations of several species across their Pacific range. However, the patterns of gene flow do not correspond with the patterns of ocean circulation, as illustrated by allozyme analyses of A. planci, L. laevigata and three species of Tridacna (Fig. 1). Palumbi et al. (1997) have also reported that the extent of divergence of mtDNA genotypes among populations in each of four cryptic species of sea urchins {Echinometra) was not related to the ocean surface flows connecting those populations. They suggested that stochastic, infrequent long-distance dispersal might account for such a pattern. The most obvious mismatch between patterns of gene flow and those of presentday ocean currents, however, was that de- scribed for giant clams (Fig. 1). This is partly because sampling density and sample distribution were sufficient to determine the main paths of gene flow, and to test their congruence with ocean circulation patterns. The major trends in gene flow in three different species all have an axis that trends north-west to south-east, perpendicular to the main ocean circulation which flows north-east to south-west through this region (the South Equatorial Current [SEC]). Benzie and Williams (1997) pointed out how gene flow is relatively high between the Philippines and the Marshall Islands along the equatorial countercurrent zones, where there are relatively few intervening reefs that might act as staging posts. Gene flow is limited between the Solomon Islands and the Great Barrier Reef despite the much smaller distance involved, the occurrence of many reefs that might act as intermediate sites, and the direct connection of the two areas by the SEC. In contrast, this current does not appear to entrain larvae and prevent them from dispersing between the Kiribati and Tuvalu or Cook Islands. Benzie and Williams (1997) argued why it is unlikely that giant clam larvae are transported by surface wind drift (suggested by Hale and Mitchell [1995] as the means of north-westward movement of a bacterial disease of coralline algae from the Cook Islands), by deeper present-day currents (100 m or more from the surface), or by island hopping on local currents. They considered it more likely that surface current flows at times of lowered sea level flowed parallel to the island chains to a greater extent than today, and that the patterns of gene flow in the giant clams reflected past dispersal. Recent data from the starfish Linckia laevigata is of interest, because this species displays no significant spatial variation in allozyme frequencies, consistent with high dispersal throughout the species' Pacific range (Williams and Benzie, 1996). However, significant differentiation of the frequencies of mtDNA genotypes demonstrated greater connectivity between the Philippines and Western Australia, and between the Great Barrier Reef and Fiji, than among any other pairings of these populations (Williams and Benzie, 1997). These results 133 CORAL REEF GENETICS: GHOSTS OF DISPERSAL PAST Marshall Is. Kiribati Soiamon\Tuva|u Number of migrants per generation <2 2-5 FIG. 1. Patterns of gene flow among populations of the starfish Acanthaster planci (after Benzie, 1998) and Linckia laevigata (after Williams and Benzie, 1997, 1998) in the Indian and Pacific Oceans, and among populations of giant clams Tridacna maxima, T. gigas and T. derasa (after Benzie and Williams, 1997) in the western Pacific, illustrating the lack of concordance of the patterns of gene flow with major surface ocean circulation. suggested that the allozymes were not at equilibrium, and their lack of spatial structure reflected past dispersal events rather than present-day gene flow. The greater connectivity of populations on either side of the New Guinea/Australia axis, rather than between the Great Barrier Reef and the Western Australian populations, suggested that the patterns of mtDNA gene flow reflected routes existing at times of low sea level when Australia and New Guinea were joined by a land bridge. It is clear that while there may be high gene flow today among L. laevigata populations in strongly connected reef systems such as the Great Barrier Reef, the genetic uniformity over the Pacific is the result of past dispersal. These data are of interest be- cause they also suggest that species for which allozyme data show little or no genetic structure, and which would have been interpreted in the past to imply high present-day gene flow, may reflect past pulses of dispersal—such patterns may best be described as the ghosts of dispersal past. Further evidence for lowered sea levels affecting the genetic structure of Indo-Pacific marine species comes from comparison of Indian and Pacific Ocean populations. These oceans were largely cut off from each other during each glaciation as sea levels dropped up to 130 metres below present-day levels (Haq et al., 1987; Chappell et al., 1996). The narrow seaways which remained were also likely to have been much cooler as a result of upwellings, 134 JOHN A. H. BENZIE further preventing the dispersal of warm water tropical species between the oceans (Potts, 1983, 1985; McManus, 1985; Fleminger, 1985). The strength of the pattern is obvious in illustrations of the variation in allele frequencies among populations of the starfish, L. laevigata and A. planci, and the mangrove species, Avicennia marina (Fig. 2). All of these species show concordant patterns of allozyme variation at several loci indicating a marked change in allele frequencies where the Indian and Pacific Oceans meet. The allozyme data from Av. marina (Duke et al, 1998) and A. planci (Benzie, 1999) also show a genetic distinction between North and South Pacific populations (Fig. 2). These data suggest that not only were the Indian and Pacific Oceans isolated, but that regions within each were also isolated, possibly indicating several refugia in each ocean at low sea-level stands. Populations showing a similar genetic signature often range over several degrees of latitude and do not appear to show any relationship to environmental circumstances (Williams and Benzie, 1998). The lack of gene exchange between groups may reflect a degree of co-adaptation among different genes, or particular patterns of epistasis (gene interactions) that are stable within each group, but break down on interbreeding between groups. Each group is therefore well-adapted to the environmental conditions throughout their range, and could equally survive in new habitats. However, the genetic construction within each group prevents the re-integration of the gene pools. Lessios and Weinberg (1993) have provided an interesting case study of the extent to which gene flow in tropical marine isopods is affected by the populations already occupying a site and the extent to which they are able to mate effectively with any immigrants, and the role that differences in their genetic constitution can play in this process. Burton (1987) has also demonstrated the powerful structuring among copepod local populations on the west coast of North America that persist in the face of apparently high dispersal and appear to be related to co-adapted complexes or groups of genes with stable epigenetic interactions. Genetic mechanisms that more rapidly homogenise variants within such groups, such as molecular drive (Dover, 1982), might also play a role, although no evidence has yet been collected from Indo-pacific taxa to test this point. The degree of genetic differentiation among populations of the starfish L. laevigata, A. planci, and Av. marina in different oceans is an order of magnitude more than that occurring among populations within either ocean. Similar differences have been reported for butterfly fish, Chaetodon spp., (McMillan and Palumbi, 1995) and the coconut crab, B. latro, (Lavery et al., 1996) and non-reef coastal fish (Chenoweth et al., 1998) and prawns (Benzie et al, 1992). The geographical separation of the coral reef species samples has often been too great to assess the nature of the interaction between the Indian and Pacific populations after the reunion of their ranges. However, Chenoweth et al. (1998) provide evidence of secondary inter-gradation between the sea bass populations they studied, suggesting dispersal from east and west with genotypes mixing over northern Australia. Benzie et al. (1992) have evidence of migration from the east as far as western Australia, in prawns. Changing sea level as a result of glaciation has therefore had a significant and lasting effect on the genetic structure of tropical marine species through changing the geographic and oceanographic barriers to dispersal and gene flow. FIG. 2. Spatial variation in the allele frequencies of representative loci from the starfish Acanthaster planci (after Benzie, 1998) and Linckia laevigata (after Williams and Benzie, 1998), and the mangrove tree, Avicennia marina (after Duke et al.. 1998) illustrating the marked shift in the genetic constitution of populations between the Indian and Pacific Oceans. Note that Western Australian populations of all three species have a genetic constitution consistent with a Pacific origin, and that there is evidence for a division of southern from northern Pacific populations of A. marina and A. planci. CORAL REEF GENETICS: GHOSTS OF DISPERSAL PAST ENOL* 113 100 Other B 135 136 JOHN A. H. BENZIE Divergence times of populations and Divergence times between many species in the Caribbean and the Pacific are similar molecular phytogenies In this section, the times of divergence of to those in the Indo-Pacific, but are likely populations or species of coral reef organ- to have been dominated by the tectonic events that uplifted the Isthmus of Panama. isms is reviewed. The time of divergence of However, it is worth noting that some aua group of populations belonging to differ- thors have suggested that a number of enent species does not necessarily imply the vironmental changes of the type that are time of speciation. Here, the approach is not also associated with climate change, such particularly concerned about speciation per as current changes and upwellings, may se—more about the timing of the genetic have influenced speciation prior to the sepdivergence of populations whether within aration of the Pacific and the Caribbean by taxa or between them. land masses (Knowlton et al, 1993; JackEstimates of the times of divergence of son et al, 1993). The data for the butterfly populations or species across the Indian/Pa- fish (McMillan and Palumbi, 1995) also cific Ocean divide demonstrates that all are demonstrate that speciation has occurred relatively young and less than 1—3 million within each of the Pacific and Indian ocean years old (Table 1). The genetically differ- basins on a similar time scale (Table 1). In entiated clam stocks on different island fact, good species that have relatively few chains show divergence times which range genetic differences between them, implying from 0.1-1.5 Ma, as do estimates for pearl rapid speciation, are documented in Linckia oysters distributed among the same island (L. laeviagata and L. multifora [Williams, chains (Table 1). Divergence times between 1997]) and Acanthaster (A. planci and A. Indian and Pacific Ocean populations, and brevispinus [Benzie, 1999]). Echinometra closely related species of butterfly fish species have also arisen within the last 1—2 million years within the Pacific basin (Palrange from 0.18-2.00 Ma. An important exception are the available umbi, 1997). data for corals. These indicate divergence The molecular data cannot be used to artimes much greater than those for other taxa gue that all species in reef systems are of (7.60-23.00 Ma). Potts (1983, 1985) and recent origin, but the overwhelming preVeron (1995) have argued how relatively ponderance of recent divergences between little speciation might be expected in corals the taxa that have been investigated is inbecause of the long generation times of triguing, and suggests a dominant role of these colonial organisms compared with recent events. This time period still covers time scales of recent sea level changes. millions of years, and there have been a vaPotts and Garthwaite (1991) note more re- riety of divergence times estimated, implycent divergence times for shorter-lived Por- ing that divergence, and, a separate event, ites species (<2.0 Ma) consistent with that speciation, do not appear to have occurred for the other coral reef species with similar at one and the same time for all taxa. The generation times given in Table 1. Chen and genetic divergence of populations often folMiller (1996) consider the sequence diver- lows separation by some barrier, and in the gence between Caribbean and Indo-Pacific case of the Indo-Pacific, the major barriers species of Rhodactis (Coralliomorphs) to appear to be a combination of land masses reflect divergence from 3.1—3.5 million and upwellings that are associated with mayears and that among Indo-Pacific species jor changes in global climate that result in to be less, but do not give a time estimate changes in sea level and ocean circulation. based on molecular data alone. Similarly, Isolation across the Isthmus of Panama has although ITS regions have been used to as- largely resulted from the tectonic uplift of sess relationships among Acropora species, that land barrier, but there is also evidence the assessment of divergence times was that changes in sea level and upwellings ascomplicated by the occurrence of reticulate sociated with climate change have also inexchange among taxa (Odorico and Miller, fluenced the isolation and genetic divergence of marine species. 1997). * Excludes Western Australian populations. Atpheus spp. Eucidaris spp. Echinometra spp. Between species (between oceans) Chaetodon (punctofasciatus group) Chaetodon (rhombochaetodon group) Diadema spp. Chaetodon (punctofasciatus group) Chaetodon (rhombochaetodon group) Chaetodon (rhombochaetodon group) Poriles spp. Porites spp. Goniopora spp. Echinometra spp. Birgus latro Avicennia marina Between species (within oceans) Linckia laevigata/Linckia multifora Indian/Pacific Indian/Pacific Eastern Pacific/Caribbean Eastern Pacific/Caribbean Eastern Pacific/Caribbean Eastern Pacific/Caribbean Knowlton et al, 1993 Bermingham and Lessios, 1993 Bermingham and Lessios. 1993 McMillan and Palumbi, 1995 McMillan and Palumbi, 1995 Bermingham and Lessios, 1993 McMillan and Palumbi, 1995 McMillan and Palumbi, 1995 McMillan and Palumbi, 1995 Potts and Garthwaite, 1991 Garthwaite et al., 1994 Garthwaite et al, 1994 Palumbi, 1996 Williams, 1997 Indian and Pacific Pacific Ocean Pacific Ocean Indian Ocean Caribbean Sea Western Pacific Western Pacific Pacific Ocean Lavery et al., 1996 Duke et al, 1998 Indian/Pacific Indian/Pacific Benzie, 1999 Williams and Benzie, 1998 Population groups within species (between oceans) Acanthaster planci Indian/Pacific Linckia laevigata Indian/Pacific Source Benzie and Williams, 1995 Benzie and Williams, 1997 Macaranas et al, 1992 Benzie and Bailment, 1994 Lavery et al., 1996 Duke et al., 1998 Benzie, 1999 Williams and Benzie, 1998 Geographical region Population groups within species (within oceans) Western Pacific Tridacna gigas Western Pacific Tridocna maxima Western Pacific Tridacna derasa Western Pacific Pinctada margaritifera Western Pacific Birgus latro Western Pacific Avicenma marina Indian Ocean Acanthaster planci* Indian Ocean Linckia laevigata* Population or taxon mtDNA (cyt b) mtDNA (cyt b) Allozymes (34 loci), (whole genome) Allozymes (31 loci), (whole genome) Allozymes (25 loci), (whole genome) Allozymes (16 loci), (COI) mtDNA mtDNA mtDNA mtDNA Allozymes (16 loci), mtDNA (COI), nuclear 18s rRNA gene. mtDNA (cyt b) mtDNA (cyt b) mtDNA (cyt b) Allozymes (14 loci) Allozymes (13 loci) Allozymes (13 loci) mtDNA (COI) Allozymes (9 loci) Allozymes (7 loci), mtDNA (12S, 16S, tRNA,hr, RNAglu) mtDNA (whole genome) Allozymes (11 loci) Allozymes (7 loci) Allozymes (6 loci) Allozymes (9 loci) Allozymes (7 loci) mtDNA (whole genome) Allozymes (11 loci) Allozymes (9 loci) Alozymes (7 loci), mtDNA (12S, 16S, tRNAlhr, RNAglu) Type of molecular data 3.30-9.60 3.29 2.99-4.04 0.80-2.00 0.80-2.00 2.64 0.26-0.87 £0.87 0.34-0.87 <1.00 7.60-22.30 3.50 1.00-3.00 <0.18 0.56-1.40 0.20-2.00 1.60 0.79 0.14-0.42 0.90-1.50 1.53 0.80 0.20-0.50 2.00 0.30 0.24 Time of divergence (My) TABLE 1. Age of divergence of genetically differentiated populations, or of species and genera of coral reef species, derived from molecular data. Data are those reported in the source, or calculated from genetic distances or sequence divergences provided in the sources assuming a 2% sequence divergence of mtDNA every million years, or assuming divergence time equalled Nei's D times 5 X 106 (see Avise [1994, pp. 104]) for a discussion on molecular clocks). CO _j r m CO o O on O xo 1o w O Ti w tn r 70 70 oO 138 JOHN A. H. BENZIE Non-molecular data from molluscs also underscore the high degree of speciation in reef systems in the Pleistocene. Data summarized by Kohn (1985) from the genus Conus, one of the few groups for which a sound taxonomy and fossil record exist, show a high degree of speciation in reef species relative to the non-reef species that has occurred in the last 3 million years (Table 2). It was suggested by Kohn that habitat heterogeneity and the species diversity (leading to more complex community structuring) in coral reef systems was responsible for higher rates of speciation. Although preliminary, Kohn noted the consistency of the results over a wide geographical area, and the reliability of the fossil record then known. Since that work, Jackson et al. (1993) have noted the high rates of generation of new species of strombids in the Caribbean over the last 3 million years and Kay (1996) has discussed the high rates of cowrie speciation in the Pacific during the Pleistocene. Much of the genetic structure within species, and many speciation events in tropical marine faunas, have their origin in relatively recent geological time (<3 Ma). They do not reflect ancient relationships derived from vicariant separation of parts of the Tethys Sea 20-30 Ma ago. Information from fossil molluscs suggests that reef environments were particularly conducive to speciation, and therefore have played an important role in the generation of biodiversity. Biogeography and distribution patterns of molecular variants Two main views have dominated thinking on the origin of coral reef faunas and floras in the Indo-Pacific, although there are many variants on these main themes (Rosen, 1984, 1988; Veron, 1995). The first is that species originate within a centre of origin in the Indo-West Pacific region, marked by its high biodiversity, and disperse outwards into the ocean basins with species diversity declining with distance into the ocean. The second is that species originate in the ocean basins and produce a region of high biodiversity through 1) overlap of distributions of Indian and Pacific "S 8 s 1£ s o o E o •a s sg; !.S 8 8J •2 s 5g e 'g 8. §1 a t 3 = J u 5 c 3 o ei Z CORAL REEF GENETICS: GHOSTS OF DISPERSAL PAST 139 Ocean species or, 2) accumulation of spe- rived genotypes. These data suggest a pricies in the region of high diversity. The mary evolution in the east and movement Indo-west Pacific region is thought to have westwards and is, therefore, inconsistent extensive areas of suitable habitats to main- with the centre of origin idea. tain sufficient population sizes of most speAlthough Benzie and Williams (1997) cies, in contrast to the ocean basins where considered that the patterns of gene flow in small islands have fewer habitats and small- giant clams were consistent with eastward er areas of any given habitats. Extinction movement from the Indo-West Pacific, Benrates are therefore thought to be higher in zie (1998) noted that the mechanisms of the ocean basins. dispersal identified (whether sea-surface The biogeographical implications of mo- microlayer drift or palaeocurrents) provided lecular data have been reviewed recently by for stronger migration to the northwest and Palumbi (1997) and Benzie (1998). Pal- therefore from the Pacific towards Indoneumbi (1997) notes the difficulty of testing sia. The detection of blocks of populations biogeographical hypotheses because of the which show strong connectivity and cover fact that many have similar predictions for large areas of ocean, and which have dispatterns of genetic diversity for the Indo- junct distributions (Benzie and Williams, Pacific. Nevertheless, Palumbi et al (1997) 1997; Palumbi et al, 1997; Benzie, 1999; have described mtDNA genotypes (haplo- Duke et al, 1998; Williams and Benzie, types) or mtDNA clades which occur in 1998), is not consistent with a dominant only one population (and are therefore role of eastward movement from the Indoknown as private haplotypes or private West Pacific. They suggest the existence of clades) of Echinometra throughout the Pa- several areas of relatively independent evocific. They suggested that unique mtDNA lution, possibly refugial areas at times of types are able to evolve and accumulate low sea-level stand. anywhere in the Pacific, so dispersal from The subdivision of the Indonesian region a centre of speciation in the Indo-West Pa- during times of low sea level into several cific is not a necessary requirement to ex- sea basins and the likely impetus to speciplain Indo-Pacific biogeography. ation in that region has been emphasised in Palumbi (1997) has also suggested that the past (Potts, 1983, 1985; McManus, higher extinction rates in peripheral areas of 1985). However, much coral reef habitat is the Pacific can explain the reduced species lost in that region as coastal shelf becomes diversity, and reduced genotypic diversity land, and, conversely, coral habitat in the in those regions but says nothing about the ocean basins, and connectivity between recomposition (ancestral/derived) of the ge- gions within the ocean basins, may have innotypes represented. In the absence of any creased with the appearance of new islands other influence, extinctions should lead to and reef areas (Kleypas, 1997; Kleypas et both ancestral and derived genotypes being al, 1999; Paulay, 1990; Paulay and Mcfound throughout the Indo-pacific. Palumbi Edward, 1990). These may well form inet al. (1997) illustrated an example from E. dependent areas of evolution, providing oblonga where the derived mtDNA geno- substantial metapopulation sizes. During types are found in the Indo-West Pacific, sea level rise some range expansion may but the basal types from which they arose occur, including immigration into the Indoare found in the eastern and central Pacific West Pacific centre of diversity, but the ex(Fig. 3). This pattern could only result from tent of genetic mixing will be determined extinction rate differences if higher extinc- by the degree of genetic change, or co-adtion rates preferentially removed derived aptation in the genetic architecture, that has genotypes. If extinction rates were higher occurred within the different refugia. in the Pacific basin, as has been suggested, The molecular data add to other evidence one might expect fewer ancestral, or at least which contradicts the centre of origin hyvery old, genotypes in that region as they pothesis as the dominant process controlwould have had to have survived extinction ling Indo-Pacific biogeography. The occurfor far longer periods than more recent derence of endemic species throughout the 140 JOHN A. H. BENZIE Symphyllia and Coscinaraea Echinometra oblonga private haplotype O private clade • Okinawa Hawaii Papua New G u i n e a / ' Derived Echinometra oblonga Basal FIG. 3. Sites of origination of derived genotypes and species. Top left: An area cladogram based on the relationships among species from the coral genera Symphyllia and Coscinaraea, illustrating the closest relationship occurs between geographically neighbouring regions, and that recent evolution has occured in the Pacific, far from the Indo-West Pacific centre of coral diversity (after Pandolfi, 1992). Top right: The position of mtDNA genotypes (haplotypes) or mtDNA clades which occur in only one population (and are therefore known as private haplotypes or private clades) of the sea urchin Echinometra oblonga throughout the Pacific. Bottom: The distribution of mtDNA haplotypes of E. oblonga in the Pacific, illustrating the derived nature of the genotypes in the Indo-West Pacific relative to those in the central and eastern Pacific (after Palumbi, 1997). Pacific had been used by a number of work- out the Pacific, that migration probabilities ers to suggest species arose in the Pacific were related to ocean circulation and that and not in SE Asia, but particularly in pe- extinction occurred when no species were ripheral areas of the Pacific (Ladd, 1960; found in a region at the end of an iteration Kohn, 1985; Kay, 1984; Springer and Wil- of the model (a region being the cells liams, 1990). Jokeil and Martinelli (1992) shown in the Fig. 4). They demonstrated an developed models assuming speciation oc- accumulation of diversity in the Indo-West curred in (undefined) marine taxa through- Pacific, very similar to that recorded for CORAL REEF GENETICS: GHOSTS OF DISPERSAL PAST 141 of species ranges and accumulation of taxa in the SE Asian region. GENERAL DISCUSSION Vortex Model ami 50°. Number of species present ^ ^ | > 200 FIG. 4. Results of the Vortex Model in which species number was initially set at ten species per grid box. Species were dispersed to adjacent boxes with a high medium or low probability depending on the direction of prevailing ocean currents. Speciation and extinction was assumed to occur throughout the Pacific and these events were assigned at random, except when a box reached zero species, when extinction and speciation could no longer occur (after Jokiel and Martinelli, 1992). Over 160 iterations, a pattern of high diversity in the Indo-West Pacific developed, similar to that observed for coral reef species (Veron, 1995). coral species (Veron, 1995) (Fig. 4). Pandolfi (1992) has demonstrated that some of the most derived species of coral in the genera Symphyllia and Coscinaraea are found in the Pacific and not SE Asia, consistent with the origination of species in the ocean basins (Fig. 3). Wallace (1997) has provided evidence that endemic coral species occur in the Indian and Pacific oceans as well as the Indonesian region, and that the high diversity in the latter area reflects overlap Over the 100's of millions of years of the earth's history, there have been marked changes in the nature and composition of the biota associated with carbonate reefs (Veron, 1995; Potts, 1999). These changes have occurred relatively rapidly after long periods in which the major biota remain unchanged, and all follow periods of marked, and relatively rapid, change to the global environment. The present-day biota associated with coral reefs first became dominant 230 Ma ago. Pandolfi (1999) shows that, at least over the last million years or so, the same communities recur despite the major climatic changes ocurring during the ice ages. This suggests that coral reef communities are relatively resilient (see Done, 1999; Lasker and Coffroth, 1999), have survived previous global climate change, and appear likely to survive future changes. The molecular data show that the genetic structure of reef species appears to have been determined by different current patterns than those prevailing today. The lack of congruence with present day surface circulation does not imply that genetic structure results only from past events. It may suggest that present-day mechanisms of dispersal are different from those assumed to have been the case so far. However, Benzie and Williams (1997) considered the possibilities for alternative dispersal mechanisms and found none for which there was compelling evidence to suggest their dominance today. Palumbi et al. (1997) also suggest rare, intermittent pulses of long distance dispersal (by means undefined) best explained the patterns of genetic variation they observed in Echinometra—and this also means the observed pattern is a result of an event some time in the past. Thus, spatial patterns of genetic divergence not associated with present-day ocean circulation suggest the evolution of isolated populations in different parts of the Pacific, with occasional long-distance dispersal. The data are sparse but suggest the existence of multiple refuges, and that the pattern of genetic variation are set at the time 142 JOHN A. H. BENZIE ConnectivityThrough Time 150 -150 -100 -50 0 Relative Sea Level (m) FIG. 5. A schematic representation of the distribution of a hypothetical taxon, and its response to repeated isolation over the last 150,000 years of changing sea level. Populations are subdivided, may coalesce when gene flow is re-established, or they may have accumulated sufficient genetic change that gene flow between groups is highly restricted. The figure illustrates that at least some of genetic changes to the populations that apparently have restricted gene exchange present-day were first established long before the latest isolating events 18,000 years ago at the last glacial maximum (Haq et al., 1987; Chappell et ai, 1996). of intermittent dispersal or soon after. This is most likely to have occurred during range expansion. The role of historical factors, and past dispersal events, have been considered important in determining the genetic structure of terrestrial faunas and floras (Hewitt, 1993, 1996). Large regions are occupied by populations having a particular set of genotypes, and little genetic differentiation among populations, and are separated from other such groups by sharp borders, and sometimes by narrow hybrid zones, as il- lustrated by detailed work on grasshoppers, ferns and conifers. Work by Hewitt and coworkers has explicitly considered how range expansion into areas from which a species is absent may result in rapid and extensive gene flow, while gene flow may be much reduced in dense populations as a result of competition. For example, when trees are few and far between at the edge of an expanding range, successful fertilization involves pollen travelling some distance, and the resulting seeds may travel some distance to colonise new ground. CORAL REEF GENETICS: GHOSTS OF DISPERSAL PAST However, in a dense tree stand most pollen is trapped by near neighbours and seeds may not travel so far and fewer may establish themselves in the face of strong competition from other seedlings. The timing of the divergence of population groups/species (most within the last 3 million years) is usually far greater than the last low sea level stand (18,000 years ago [Haq et al, 1987; Chappell et al, 1996]). The original differences may have developed over a short time in some instances, perhaps only a few thousand years, while in others, populations may have successfully re-integrated after a number of separations (Fig. 5). However, because there have been repeated cycles leading to the same or similar patterns of range disruption, the divergences at some loci will have arisen much earlier than the latest low sea level stand. This suggests the genetic structure was reinforced during repeated cycles of range retraction and expansion, with little change in geographical pattern occurring from when it was first set. These findings have much in common with those described in greater detail for terrestrial faunas that have invaded northern regions after the retreat of the ice caps (Hewitt, 1993, 1996). Evidence of repeated range contraction and expansion, often from the same refugia, and of sharp borders between genetic groups developing repeatedly in the same geographical zones has been described for grasshoppers. Data on molecular population genetics of coral reef organisms over ocean scales have been obtained relatively recently, but have already revealed unexpected results that raise questions about our understanding of the mechanisms giving rise to, and maintaining, genetic diversity in the Indo-Pacific. They indicate that: 1) global climate change during the Pleistocene, and its effects on sea level, have had a dramatic and lasting effect on coral reef species, 2) these events have played an important, if not dominant, role in determining the genetic diversity of tropical marine species observed today, and 3) they are not consistent with dispersal from an Indo-West Pacific centre of origin, but provide some evidence for evolution in the ocean basins and dis- 143 persal towards the Indo-West Pacific centre of diversity. Much of this evidence has not come from corals themselves but from species living in coral reef systems. However, many of these species share the same general environments and life histories (with respect to larval phases and dispersal modes) with corals. There is some evidence that corals as a group may take longer to diverge genetically as a result of their long life span and clonal nature, but where the have a life cycle similar to other reef organisms they follow the same trend. It is likely that much of the taxonomic confusion in corals arises from spatial heterogeneity induced by vicariant separation of populations at times of low sea level, and subsequent partial re-integration. The patterns of genetic divergence suggest several centres of recent evolution in coral reef species, particularly during low sea level stands. The range expansions and reductions do not appear to be dominated by a pattern of refugia based on the Indo-West Pacific region of high diversity, but provide evidence for recent regional evolution within the ocean basins. Once established, these patterns appear to be maintained for several thousands of years, suggesting little effective gene flow among those groups today under conditions of the recent past. As the diversity of coral reef ecosystems is influenced to a considerable degree by regional biodiversity (Karlson and Cornell, 1999), the factors influencing the generation of patterns of genetic variation also have important consequences for community diversity. With respect to the response of coral reef communities to global climate change it is clear that the extent to which reef biodiversity is likely to survive future change will depend on the extent to which future impacts mirror those in the past. If the geographic pattern, number, or scale of refugia are markedly different under a scenario of increasing CO2, decreased calcification rates, and local human impacts, marked changes in the nature and pattern of biodiversity of coral reef organisms can be expected. 144 JOHN A. H. BENZIE Vicariance and interchange in marine invertebrates. In B. Schierwater, B. Streit, G. P. Wagner, This is contribution number 945 from the and R. 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