Download Evidence for Sympatric Speciation by Host Shift

Current Biology, Vol. 14, 1498–1504, August 24, 2004, 2004 Elsevier Ltd. All rights reserved.
DOI 10.1016/j .c ub . 20 04 . 08 .0 2 9
Evidence for Sympatric Speciation
by Host Shift in the Sea
Philip L. Munday,1,* Lynne van Herwerden,1
and Christine L. Dudgeon2
1
Centre for Coral Reef Biodiversity
School of Marine Biology and Aquaculture
James Cook University
Townsville, QLD 4811
Australia
2
School of Life Sciences
University of Queensland
St. Lucia, QLD, 4072
Australia
Summary
The genetic divergence and evolution of new species
within the geographic range of a single population
(sympatric speciation) contrasts with the well-established doctrine that speciation occurs when populations become geographically isolated (allopatric speciation). Although there is considerable theoretical
support for sympatric speciation [1, 2], this mode of
diversification remains controversial, at least in part
because there are few well-supported examples [3].
We use a combination of molecular, ecological, and
biogeographical data to build a case for sympatric
speciation by host shift in a new species of coraldwelling fish (genus Gobiodon). We propose that competition for preferred coral habitats drives host shifts
in Gobiodon and that the high diversity of corals provides the source of novel, unoccupied habitats. Disruptive selection in conjunction with strong host fidelity could promote rapid reproductive isolation and
ultimately lead to species divergence. Our hypothesis
is analogous to sympatric speciation by host shift in
phytophagous insects [4, 5] except that we propose
a primary role for intraspecific competition in the process of speciation. The fundamental similarity between these fishes and insects is a specialized and
intimate relationship with their hosts that makes them
ideal candidates for speciation by host shift.
Results and Discussion
Habitat specialization, competition for limited resources, and assortative mating according to habitats
provide conditions conducive to sympatric speciation
by host shift [1, 2, 5]. Species of Gobiodon satisfy all
these characteristics. These small (⬍60 mm total length)
fishes live among the branches of live corals and rely
on their host coral for shelter, breeding sites, and in
some cases a source of nutrition [6, 7]. All species of
Gobiodon have a specialized pattern of host use and
prefer to occupy just a few species of coral over all
others available on the reef [6, 8]. Coral hosts are in
limited supply and experimental manipulations have
*Correspondence: [email protected]
demonstrated that there is intense competition for colonies of preferred coral hosts [9, 10]. Therefore, individuals that shift to an unexploited coral host could benefit
from reduced competition and have relatively high fitness even if they were initially poorly adapted to the
new habitat. Because of the great diversity of corals
present on reefs, there are a range of unexploited coral
species at any location that provide the opportunity for
host shifts. Finally, there is potential for the development
of reproductive isolation among individuals occupying
different host species, because adults exhibit extreme
fidelity to their host corals [11], and juveniles settle on
the same host species as adults [6, 10]. Adults rarely
move among coral colonies and most individuals spend
their entire reproductive life in the same coral colony
(P.L.M., unpublished data). The combination of these
key elements in the ecology of coral-dwelling gobies
provides the raw material for sympatric speciation by
host shift.
Here, we describe the evolution of a new species of
coral-dwelling goby (Figure 1A) that is known from just
one locality in southern Papua New Guinea. This undescribed species is currently referred to as Gobiodon
species B [7], but for simplicity it will be referred to here
as “new species”. Extensive sampling of coral gobies
in Papua New Guinea and on the Great Barrier Reef,
Australia by one of the authors (P.L.M.) indicates that
this species has a very small geographic range centered
around Bootless Bay in southern Papua New Guinea [7,
8]. At that locality, a viable population of several hundred
individuals has been observed over a period of eight
years (P.L.M., unpublished data). Social groups of up to
ten juveniles and adults are found together exclusively
inhabiting the coral, Acropora caroliniana.
The new species shares a distinctive down-turned
lower jaw with G. brochus (Figure 1B, [12]) and another
undescribed species, Gobiodon species A (Figure 1C).
The bright green and red body coloration of the new
species is very similar to that of G. species A and two
other species, G. histrio and G. erythrospilus (Figures
1D and 1E) but is unlike that of G. brochus. All these
species occur together on reefs in southern Papua New
Guinea and with the exception of the new species, have
distributions that extend throughout much of the tropical
western Pacific [7, 12–14].
Our molecular analysis shows that the new species
is closely related to Gobiodon species A (Figure 2) and
that the two species diverged between 0.18 and 0.72
million years ago (MYA). The estimated date of divergence is between 0.64 and 0.72 MYA when we use a
mutation rate of 3.6% per million years calculated in
previous studies where geological events were available
to calibrate the rate of D-loop divergence in marine [15]
and freshwater fishes [16]. However, considerable variation in D-loop mutation rates has been reported among
fishes, and this estimate is likely to be highly conservative. The estimated date of divergence is much more
recent, between 0.18 and 0.20 MYA, when we use a
D-loop mutation rate of 12.9% per million years that
Sympatric Speciation in the Sea
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Figure 1. Species of Coral-Dwelling Goby (Genus Gobiodon) that
Occur Together on Reefs in Bootless Bay, Papua New Guinea
Gobiodon new species (A), G. brochus (B) G. species A (C), G. histrio
(D) and G. erythrospilus (E).
has been reported in other fishes [17] for a comparable
region of D-loop to that used here.
The ecological and biogeographical data indicate that
this new species might have evolved by a host shift in
sympatry from the ancestral Gobiodon species A. First,
for species in this clade, the ancestral pattern of host
use is to inhabit a range of coral species that always
includes Acropora tenuis (Figure 2); however, the new
species uses just one novel species of coral, A. caroliniana (Figure 2). Speciation by host shift in sympatry requires a well-defined change in host use of the type
observed here. In contrast, if speciation occurred in
allopatry, the new goby species would be expected to
retain the ancestral pattern of host use and at least
inhabit A. tenuis. Second, A. caroliniana is not inhabited
by any other species of coral-dwelling goby [7, 8] and,
therefore, would have been vacant prior to the host shift
and provided a refuge from both intra- and interspecific
competition. Third, field observations and experiments
have demonstrated that host corals are a limited resource for coral-dwelling gobies [6, 8–10] and, therefore,
intraspecific competition for space provides a clear
mechanism driving host shifts in these species. Finally,
the known geographic range of the new species encompasses just a few hundred square km entirely within
the much larger range of G. species A [7, 14], which is
consistent with a sympatric mode of speciation.
Comparisons of host use, geographical distributions,
and relative time since divergence are also consistent
with a host shift in sympatry. The new species has a
very small geographic range [7], which corresponds with
the relatively recent divergence from G. species A (Figure 2). The host coral used by the new species, A. caroliniana, is restricted to the Indo-Australian archipelago
and is uncommon throughout most of its range, but is
locally abundant in Papua New Guinea [18]. The relatively high abundance of A. caroliniana in southern Papua New Guinea would provide the opportunity for a
host shift and sufficient habitat to support a viable population. The scarcity of A. caroliniana elsewhere might
have then limited the potential for range expansion by
the new species. G. species A and G. brochus have
much larger geographic ranges than the new species,
including much of the Indo-Australian archipelago and
tropical western Pacific [7, 12, 14]. These larger geographic ranges correspond with a more ancient divergence (between 0.95 and 4.2 MYA) of G. brochus (Figure
2) and the broad range of their shared host, A. tenuis
[18]. G. histrio and G. erythrospilus diverged even earlier
and prefer a host coral, A. nasuta, that is widely distributed throughout the Indian and Pacific Oceans [18]. As
expected, G. histrio and G. erythrospilus appear to have
the largest geographic ranges of the species considered
here, extending throughout the Indo-Pacific archipelago
and into the Indian and central Pacific oceans [6, 7,
13, 14].
Sympatric speciation is favored among habitat specialists, such as coral gobies, where there are opportunities for some individuals to occupy novel hosts. However, for divergence to occur, the use of a novel host
must be accompanied by a mechanism, such as assortative mating, that generates reproductive isolation
[1, 2]. Because coral gobies usually breed in the same
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Figure 2. Phylogenetic Relationships, Haplotype Diversities, and Patterns of Habitat
Use of Gobiodon Species
The rooted phylogram of ML phylogenetic
analysis, with Paragobiodon xanthosomus as
outgroup, shows only interspecies nodes
(see Figure 3 for complete phylogram). Also
shown are the haplotype network and pattern
of host use for each species. Collection location for specimens used in the haplotype digram are the same as for Table 1. n ⫽ number
of specimens analyzed for haplotype diagram. Circles depict individual haplotypes,
and circle sizes are relative to numbers of
individuals sharing a haplotype. The smallest
circles represent single individuals, and the
largest circle represents eight individuals.
Lines with crossbars connect haplotypes in
each network to each other. The number of
crossbars indicates numbers of base changes
(substitutions) between haplotypes. Numbers
of unique haplotypes and numbers of substitutions are used to calculate nucleotide and
haplotype diversity indices in Table 1. The
complete phylogram (Figure 3) indicated that
there was no geographic differentiation within
species clades; therefore sampling from several locations did not confound the phylogenetic relationships between spp. Patterns of
host use exhibited by each species are indicated to the right of the species names.
Graphs of host use show percent of different
host species inhabited in southern Papua
New Guinea [8].The abbreviations are as follows: D, Acropora digitifera; M, A. millepora;
N, A. nasuta; V, A. valida; L, A. loripes; T, A.
tenuis; C, A. caroliniana; and n, number of
gobies sampled to estimate patterns of habitat use.
host species to which they settle from the plankton, any
genetic variation that favors a shift in host use by some
settling larvae could generate assortative mating. Where
the same locus controls host prefence and perfomance
in each host, assortative mating occurs as a by-product
of specialization on different hosts [19]. This is the simplest genetic model of sympatric speciation, because a
change in the expression of just one trait (habitat choice)
by some parts of the population will automatically lead
to assortative mating of adults in different habitats. Reproductive isolation can also occur where one locus
affects host preference and another affects performance
on each host. Under strong selection, the preference locus
will rapidly become associated with the performance locus, and divergent selection on performance will drive
the reproductive isolation of populations using different
hosts [20].
We propose that frequency-dependent competition
and disruptive selection have been the principal forces
favoring a shift in host use and subsequent reproductive
isolation of the new population. Intense competition for
space is well documented in coral-dwelling gobies [8,
10]. Consequently, individuals that use an unoccupied
host species could have relatively high fitness compared
to an average individual using the traditional host. Divergent selection of phenotypes occupying each host
would then be driven by a genotype-environment interaction between performance and host use in coraldwelling gobies. Caley and Munday [21] demonstrated
that goby species with narrow habitat preferences grow
faster in the coral species they prefer to inhabit compared to coral species they inhabit less frequently. Furthermore, reproductive success of coral-dwelling gobies increases with body size of both males and females
[22]. Therefore, any trait (physiological, behavioral, or
morphological) that increases growth rate will be under
strong selection. The genotype-environment interaction
will generate disruptive selection for increased performance between the two populations of extreme specialists (the original population using A. tenuis and the new
population using A. caroliniana). Disruptive selection
could drive rapid adaptation to the new host, so that after
a few generations, individuals swapping between host
species would have low reproductive success compared to individuals remaining faithful to their host
species.
Assortative mating within habitats could be reinforced
by host recognition mechanisms. Coral gobies lay their
eggs on the host coral and the male tends the eggs until
they hatch several days later. Imprinting of the embryos
or newly hatched larvae on a novel host coral, and subsequent return of settling larvae to that species of coral,
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Table 1. Genetic Architecture of Gobiodon Species Investigated
in This Study
Species
n
nh
h
%␲
G.
G.
G.
G.
G.
10
10
13
10
10
10
9
9
5
2
1
0.87
0.83
0.7
0.32
1.93
1.23
0.89
0.41
0.10
erythrospilus
histrio
brochus
species A
new species
⫾
⫾
⫾
⫾
⫾
1.13
0.76
0.56
0.31
0.11
Values shown are the number of samples (n), number of haplotypes
(nh), haplotype diversity index (h ), and nucleotide diversity index (␲)
shown as a percentage. Samples were from Bootless Bay, PNG:
G. brochus (n ⫽ 8), G. new species (n ⫽ 10) and Lizard Island,
northern Great Barrier Reef: G. histrio (n ⫽ 10), G. erythrospilus (n ⫽
10), G. species A and G. brochus (n ⫽ 5).
would promote assortative mating. Imprinting of larvae
on their host has been demonstrated in anemone fishes
[23], another group of highly host-specific reef fishes,
and would accelerate reproductive isolation following a
host shift. Furthermore, some coral-dwelling gobies
prey on the tissue of their host corals, and preference
for the parental habitat could be passed on through
chemicals accumulated by consumption of the host.
Olfactory cues are known to influence host choices of
larval fishes when they settle from the plankton [24],
therefore, recognition of host chemistry at the time of
settlement might play a role in establishing host fidelity
and subsequent assortative mating in coral-dwelling
gobies.
Sympatric speciation by host shift appears to be the
most parsimonious explanation for the evolution of the
new species because it requires just two events to produce a new species: 1) a host shift by some settling
larvae and 2) subsequent fidelity to the new host. Allopatric speciation by peripheral isolation is also a plausible explanation but is less parsimonious, because it
would require four events to produce the new species:
1) the dispersal of a small founder population to an
isolated location, 2) addition of A. caroliniana as a host
in the new population, but not in the ancestral population, 3) loss of all ancestral hosts in the new population
and, 4) subsequent range expansion of the ancestral
species to produce the nested geographic ranges we
see today. Allopatric speciation by vicariance is even
less parsimonious because it would require five events
to produce the new species: 1) the generation of a geographic barrier that separates some part of the ancestral
population, 2) addition of A. caroliniana as a host in one
population, but not the other, 3) loss of all ancestral
hosts in that same population, 4) relaxation of the geographic barrier, and 5) range contraction in one species
and range expansion in the other species to produce
the nested ranges we see today. While both allopatric
modes of speciation are plausible, they are less parsimonious than a host shift in sympatry in this instance.
Different mechanims of speciation are predicted to
leave different signatures in the patterns of genetic diversity of sister taxa [25]. The new species considered
here exhibits very low genetic diversity (Figure 2, Table
1); much lower even than its closest relative, G. species
A, which also inhabits just one coral host, but has not
undergone a host shift. Low genetic diversity indicates
that a strong genetic bottleneck has occurred, as might
be expected following divergence of a small founder
population. Speciation by peripheral isolation of a small
population could explain the low genetic diversity observed in the new species [25]; however, this mode of
speciation does not explain why the isolated population
made a complete host shift and did not retain the ancestral pattern of host use. Furthermore, the lack of genetic
differentiation between individuals of G. brochus and
G. histrio (Figure 3) collected from locations separated
by over 1000 km (Bootless Bay and Kimbe Bay in Papua
New Guinea and Lizard Island on the Great Barrier Reef)
demonstrates that larval dispersal of these gobies can
maintain gene flow over large spatial scales. The potential for widespread larval dispersal would work against
the establishment of a small, genetically isolated (but not
geographically isolated) population in close proximity to
the parent population.
A host shift in sympatry could also explain the low
genetic diversity observed in the new species, provided
that only a small number of individuals made the host
shift and subsequent gene flow between populations
was negligible. As described above, reproductive isolation among the populations could evolve rapidly as a
result of strong disruptive selection for increased growth
rate among individuals inhabiting different host species.
Reproductive isolation would be even more rapid if it is
reinforced by host imprinting or other host recognition
mechanisms. The genetic basis for the genotype-environment interaction that favors disruptive selection may
reside in either the nuclear or mitochondrial genome.
The non-recombining mt genome (which was used as
a marker in this study) is a prime target for disruptive
selection, as it is responsible for 90% of the energetic
metabolism of the organism and as such is under strong
functional selection, with changes in the mtDNA having
substantial impacts on fitness [26].
Low genetic diversity following speciation in sympatry
could also occur if the genetic variation that favored the
host shift was pleiotropically linked to a mutation in the
mt genome that influenced performance in the new host
coral. If such an adaptive mutation occurs on the mtDNA
it may sweep to fixation carrying all linked nucleotide
variants along with it [27]. This would eliminate polymorphism, evidenced as a strong genetic bottleneck, and
maintain only those individuals in the population having
the favored mutation (and other selectively neutral mutations that may be present on the favored mt genome
[27], including the neutral section of mt DNA sampled
here).
Finally, although mitochondrial genomes are almost
exclusively maternally inherited in most eukaryotes, this
may not be the case for many fishes that are sequential
hermaphrodites. In these species all individuals will
contribute mt DNA to offspring at some stage of their
reproductive life. This effect is likely to be particularly
pronounced in coral gobies because they can swap
repeatedly between male and female function [28]. Although not formally demonstrated, hermaphroditism
may be another means by which maternal preferences
(e.g., for laying eggs on specific hosts) could spread
rapidly throughout the population, if the preference was
linked to mitochondrial type.
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Figure 3. Phylogenetic Tree of All Samples Used in the Phylogenetic Analysis of Gobiodon Species
Outgroup rooted phylogram of best tree (⫺lnL ⫽ 2791.856) from ML analysis of Gobiodon species with Paragobiodon xanthosomus as
outgroup. Numbers above branches are ML bootstrap support values, below branches are majority rule support values for 895,400 tree
topologies obtained by Bayesian inference. Sample codes indicate location sampled for each of the species as follows: G. histrio from Lizard
Island, GBR ⫽ H; from Kimbe Bay, northern PNG ⫽ HK; from Bootless Bay, southern PNG ⫽ HL; G. erythrospilus were all from Lizard Island,
GBR ⫽ E; G. brochus were from Lizard Island ⫽ BL or from Bootless Bay southern PNG ⫽ BG; G. sp. A were all from Lizard Island ⫽ GspA;
G. new sp. were all from Bootless Bay, southern PNG ⫽ Gnew.
Sympatric Speciation in the Sea
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Although we advocate a role for sympatric speciation
in the diversification of coral-dwelling gobies, we recognize that allopatric speciation has also been important
in the evolutionary history of these fishes. For example,
our analysis shows that G. histrio and G. erythrospilus
are closely related but genetically distinct (Figures 2 and
3). Although these two species have identical patterns
of host coral use, they rarely co-habit the same coral
colony and hybrids have not been observed [7, 10]. The
identical patterns of host use for these species indicates
that divergence has occurred without a shift in host use.
The most parsimonious explanation is divergence in allopatry followed by range expansions and secondary
contact. Similarly, G. brochus appears to have diverged
from the most recent common ancestor with G. erythrospilus without a host shift and current-day differences in
the relative frequency that different hosts are occupied
is largely due to the effects of interspecific competition
with G. histrio and G. erythrospilus [9].
Sympatric speciation has been largely discounted in
marine fishes because most species have a planktonic
larval phase with the potential to disperse widely and
generate genetic homogeneity over large spatial scales.
However, there is increasing evidence that larvae do not
always disperse long distances and some return to their
natal reefs [29]. Furthermore, habitat selection at settlement and assortative mating can produce reproductive
isolation at very fine spatial scales, even in species with
the capacity to disperse large distances. Clearly, a pelagic larval phase need not preclude the formation of
fine scale genetic structure because behavior can override the potential for genetic mixing [30].
Competition has long been regarded as a potent force
for ecological diversification [3] and is an explicit parameter in some mathematical models of sympatric speciation [1]. Wilson and Turelli [31] showed that a stable
polymorphism can evolve following the invasion of an
empty niche by a species experiencing strong intraspecific competition. Furthermore, their model predicts that
heterozygotes will have lowest fitness, and therefore,
that the incipient species could become reproductively
isolated as a result of disruptive selection. Recent theoretical advances [32, 33] suggest that frequency-dependent competition for a unimodally distributed resource
is sufficient to generate disruptive selection and assortative mating. In these models, disruptive selection and
assortative mating emerge as a by-product of competition and are not untested assumptions of the model. In
addition to these new mathematical models, experiments have confirmed that frequency-dependent competition can generate disruptive selection on important
phenotypic traits [34], including those involved in metabolism and growth [35]. The consensus emerging from
these theoretical and experimental approaches is that
intraspecific competition can play a key role in the divergence of new species in sympatry.
Two of the most convincing empirical examples of
sympatric speciation are the monophyletic origin of
cichlids in crater lakes in Cameroon [36] and the evolution of new host races in the apple maggot fly [37].
In both cases assortative mating of individuals using
spatially isolated resources appears to underlie population divergence. Whether intraspecific competition was
the process responsible for niche partitioning has not
been tested. Ours is one of the first empirical studies to
directly link resource competition and a experimentally
tested genotype-environment interaction to a proposed
case of sympatric speciation. Sexual selection has also
been linked to the maintenance of assortative mating
in species that appear to have diverged in sympatry
[38, 39]. However, this is unlikely to be the case for
the new species of coral-dwelling goby described here,
because there is no sexual dimorphism in this clade of
fishes [28].
In conclusion, multiple lines of evidence presented
here point to the generation of a new species of coraldwelling goby as a result of a host shift in sympatry.
Although allopatric speciation by peripheral isolation
cannot be discounted, this mechanism does not explain
the current day patterns of host use in the new species.
Our results support the emphasis given to competition
as the process underlying divergent selection and assortative mating in recent models of sympatric speciation.
Experimental Procedures
We amplified DNA (extracted from caudal fin) using universal fish
mitochondrial D-loop primers L15995 5⬘-AACTCACCCCTAGCTCC
CAAAG-3⬘ and H16498 5⬘-CCTGAAGTAGGAACCAGATG-3⬘, from all
species, except G. brochus, at an annealing temperature of 51⬚C,
in the presence of 2.5mM MgCl2. G. brochus samples were amplified
using the Universal forward primer (L15995) and a goby specific
reverse primer, GdloopR3: 5⬘-CGAAGCTTATTGCTTGCTTG-3⬘ as
described above. PCR products were directly sequenced in both
directions on an ABI 377 sequencer, using the amplification primers.
Aligned sequences (384 bp) were analyzed in PAUP* [40] following
identification of the optimal substitution model for the data using
likelihood approaches implemented in Modeltest [41], with the following specifications: ML analysis, substitution model GTR ⫹ G,
with G ⫽ 0.898, nucleotide frequencies: A ⫽ 0.382, C ⫽ 0.182, G ⫽
0.146, T ⫽ 0.291, and 100 bootstrap replicates. Trees were rooted
with Paragobiodon xanthosomus as an outgroup.
The ML tree topology was confirmed with Bayesian inference
using the program Mr Bayes [42]. A maximum likelihood model was
specified, employing 6 substitution types, with base frequencies
estimated from the data, and rate variation across sites modeled
using a ␥ distribution, G ⫽ 0.898. The Markov chain Monte Carlo
search was run with 4 chains for 1,000,000 generations, with trees
sampled every 100 generations. The first 100,000 trees were discarded as “burnin” and a majority rule consensus tree was obtained
from the remaining 900,000 trees.
The ages of divergence were calculated directly by dividing the %
genetic divergence between lineages (obtained from the ML branch
length/384 bp of sequence ⫻ 100) by the 3.6% or 12.9% per million
years divergence rates for fish D-loop sequences.
Nucleotide and haplotype diversity indices (␲ and h respectively)
of all Gobiodon species were calculated, because these indices are
expected to be less diverse in recently founded populations than
in centers of origin [43]. Nucleotide diversity indices were calculated
from sequences of all individuals sampled from PNG using the program Arlequin [44]. Haplotype diversity indices were calculated as
per Nei [45] using the formula h ⫽ n (1 ⫺ ⌺ xi2)/(n ⫺ 1).
Acknowledgments
We thank Max Benjamin, Dik Knight, Alex Anderson, Walindi Diving,
Loloata Island Resort, Mahonia Na Dari Research and Conservation
Centre, and Motupore Island Research Station for excellent logistic
support and assistance. We also thank J.H. Choat, S. Connolly, J.B.
Crespi, J. Endler, G. Jones, S. Planes, D. Schluter, S. Swearer, W.
Rice, R. Warner and three anonymous reviewers for helpful discus-
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sions and/or comments. Not all agreed with our conclusions, but
all provided insightful and helpful critique. This research was funded
by grants from the Australian Research Council and James Cook
University to P.L.M. and L.VH.
Received: February 22, 2004
Revised: June 24, 2004
Accepted: June 24, 2004
Published: August 24, 2004
22.
23.
24.
References
1. Turelli, M., Barton, N.H., and Coyne, J.A. (2001). Theory and
speciation. Trends Ecol. Evol. 16, 330–343.
2. Via, S. (2001). Sympatric speciation in animals: the ugly duckling
grows up. Trends Ecol. Evol. 16, 381–390.
3. Schluter, D. (2000). The Ecology of Adaptive Radiations, (Oxford: Oxford University Press).
4. Bush, G.L. (1969). Sympatric host race formation and speciation
in frugivorous flies of the genus Rhagoletis (Diptera, Tephritidae). Evolution Int. J. Org. Evolution. 23, 237–251.
5. Tauber, C., and Tauber, M. (1989). Sympatric speciation in insects: perception and perspective. In Speciation and its Consequences, D. Otte and J.E. Endler, eds. (Sunderland: Sinauer
Associates), pp 307–344.
6. Munday, P.L., Jones, G.P., and Caley, M.J. (1997). Habitat specialisation and the distribution and abundance of coral-dwelling
gobies. Mar. Ecol. Prog. Ser. 152, 227–239.
7. Munday, P.L., Harold, A.S., and Winterbottom, R. (1999). Guide
to coral-dwelling gobies, genus Gobiodon (Gobiidae) from Papua New Guinea and the Great Barrier Reef. Rev. fr. Aquariol.
26, 49–54.
8. Munday, P.L. (2002). Does habitat availability determine the
geographical-scale abundance of coral-dwelling fishes? Coral
Reefs 21, 105–116.
9. Munday, P.L., Jones, G.P., and Caley, M.J. (2001). Interspecific
competition and coexistence in a guild of coral-dwelling gobies.
Ecology 82, 2177–2189.
10. Munday, P.L. (2004). Competition among coral-dwelling fishes:
the lottery model revisited. Ecology 85, 623–628.
11. Nilson, G.E., Hobbs, J.P.A., Munday, P.L., and Nilsson, S. (2004).
Extreme habitat fidelity through hypoxia tolerance in a coraldwelling goby. J. Exp. Biol. 207, 33–39.
12. Harold, A.S., and Winterbottom, R. (1999). Gobiodon brochus:
A new species of Gobiid fish (Teleostei: Gobioidei) from the
western South Pacific, with a description of its unique jaw morphology. Copeia 1999, 49–57.
13. Sawada, Y., and Arai, R. (1973). Three species of coral gobies
(genus Gobiodon) from the Ryuku Islands. Japan. Bull. Natn.
Sci. Mus. Tokyo 16, 585–603.
14. Suzuki, T., Aizawa, M., and Senou, H. (1995). A preliminary review of three species of the Gobiodon rivulatus complex from
Japan. I.O.P. Diving News 6, 2–7.
15. Donaldson, K.A., and Wilson, R.R., Jr. (1999). Amphi-Panamic
geminates of Snook (Percoidei: Centropomidae) provide a calibration of the divergence rate in the mitochondrial DNA Control
region of fishes. Mol. Phylogenet. Evol. 13, 208–213.
16. Waters, J.M., Craw, D., Youngson, J.H., and Wallis, G.P. (2001).
Genes meet geology: Fish phylogeographic pattern reflects ancient, rather than modern, drainage connections. Evolution Int.
J. Org. Evolution 55, 1844–1851.
17. Alvarado, B.J.R., Baker, A.J., and Mejuto, J. (1995). Mitochondrial DNA control region sequences indicate extensive mixing
of swordfish (Xiphias gladius) population in the Atlantic Ocean.
Can. J. Fish. Aquat. Sci. 52, 1720–1732.
18. Wallace, C. (1999). Staghorn Corals of the World. (Collingwood:
CSIRO).
19. Rice, W.R. (1987). Speciation via habitat specialization: the evolution of reproductive isolation as a correlated character. Evol.
Ecol. 1, 301–314.
20. Fry, J.D. (2003). Multilocus models of sympatric speciation:
Bush versus Rice versus Felsenstein. Evolution Int. J. Org. Evolution 57, 1735–1746.
21. Caley, M.J., and Munday, P.L. (2003). Growth trades off with
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
habitat specialization. Proc. Royal Soc. London B (Suppl.) 270,
S175–S177.
Kuwamura, T., Yogo, Y., and Nakashima, Y. (1993). Sizeassortive monogamy and parental egg care in a coral goby
Paragobiodon echinocephalus. Ethology 95, 65–75.
Arvedlund, M., and Nielson, L.E. (1996). Do the anemonefish
Amphiprion ocellaris (Pisces: Pomacentridae) imprint themselves to their host sea anemone Heteractis magnifica. Ethology
102, 197–211.
Elliott, J.K., Elliott, J.M., and Mariscal, R.N. (1995). Host selection, location, and association behaviours of anemonefishes in
field settlement experiments. Mar. Biol. 122, 377–389.
Mayr, E. (1963). Animal species and evolution. (Cambridge; Harvard University Press).
Ballard, J.W.O., and Whitlock, M.C. (2004). The incomplete natural history of mitochondria. Mol. Ecol. 13, 729–744.
Rand, D.M. (2001). The units of selection of mitochondrial DNA.
Annu. Rev. Ecol. Syst. 32, 415–448.
Munday, P.L., Caley, M.J., and Jones, G.P. (1998). Bi-directional
sex change in a coral-dwelling goby. Behav. Ecol. Sociobiol.
43, 371–377.
Swearer, S.E., Shima, J.S., Hellberg, M.E., Thorrold, S.R., Jones,
G.P., Robertson, D.R., Morgan, S.G., Selkoe, K.A., Ruiz, G.M.,
and Warner, R.R. (2002). Evidence of self-recruitment in demersal marine populations. Bull. Mar. Sci. 70, 251–271.
Taylor, M.S., and Hellberg, M.E. (2002). Genetic evidence for
local retention of pelagic larvae in a Caribbean reef fish. Science
299, 107–109.
Wilson, D.D., and Turelli, M. (1986). Stable underdominance
and the evolutionary invasion of empty niches. Am. Nat. 127,
835–850.
Diekmann, U., and Doebeli, M. (1999). On the origin of species
by sympatric speciation. Nature 400, 354–357.
Doebeli, M., and Diekmann, U. (2000). Evolutionary branching
and sympatric speciation caused by different types of ecological interactions. Am. Nat. 156, S77–S101.
Bolnick, D.L. (2004). Can intraspecific competition drive disruptive selection? An experimental test in natural populations of
sticklebacks. Am. Nat. 58, 608–618.
Fresen, M.L., Saxer, G., Travisana, M., and Doebeli, M. (2003).
Experimental evidence for sympatric ecological diversification
due to frequency-dependent competition in Escherichia coli.
Evolution Int. J. Org. Evolution 58, 245–260.
Schliewen, U., Rassmann, K., Markmann, M., Markert, J.,
Kocher, T., and Tautz, D. (2001). Genetic ecological divergence
of a monophyletic cichlid species pair under fully sympatric
conditions in Lake Ejagham, Cameroon. Mol. Ecol. 10, 1471–
1488.
Filchak, K.E., Roethele, J.B., and Feder, J.L. (2000). Natural
selection and sympatric divergence in the apple maggot. Nature
407, 739–742.
Seehausen, O. Explosive speciation rates and unusual species
richness in haplochromine cichlid fishes: effects of sexual selection. Adv. Ecol. Res. 31, 237–274.
Allender, C.J., Seehausen, O., Knight, M.E., Turner, G.F., and
Maclean, N. (2003). Divergent selection during speciation of
Lake Malawi cichlid fishes inferred from parallel radiations in
nuptial coloration. Proc. Natl. Acad. Sci. USA 100, 14074–14079.
Swofford, D.L. (1989). PAUP* Phylogenetic Methods using Parsimony and other Methods. (Sunderland: Sinauer Associates).
Posada, D., and Crandall, K.A. (1998). Modeltest: testing the
model of DNA substitution. Bioinformatics 14, 817–818.
Huelsenbeck, J.P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17, 754–755.
Grant, W.S., and Bowen, B.W. (1998). Shallow population histories in deep evolutionary lineages of marine fishes: insights from
sardines and anchioves and lessons for conservation. J. Hered.
89, 415–426.
Schneider. S., Roessili, D., and Excoffier, L. (2000). Arlequin.
Vers 2.000: a software for genetic data analysis. (Geneva, Genetics and Biometry Laboratory, University of Geneva).
Nei, M. (1987). Molecular evolutionary genetics. (New York, Columbia University Press).