Download Genetic Structure of Coral Reef Organisms

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
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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
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135
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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).
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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
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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
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Corresponding Editor: Kirk Miller