© 2006 Society of Systematic Biologists
Multiple Origins of the Juan Fernández Kelpfish Fauna and Evidence for Frequent and Unidirectional Dispersal of Cirrhitoid Fishes Across the South Pacific
Edited by Adrian Patterson: Associate Editor
1 School of Life and Environmental Sciences, Deakin University, PO Box 423 Warrnambool, Victoria, 3280, Australia
2 Museo Nacional de Historia Natural Casilla 787, Santiago, Chile
3 Escuela Recursos Naturales, Universidad del Mar Amunátegui 1838, Viña del Mar, Chile
 |
Abstract |
|---|
 TopNotes Abstract Materials and MethodsResultsDiscussionAcknowledgmentReferences |
|---|
Phylogenetic relationships were reconstructed among chironemid fishes based on morphological and molecular (lrRNA, NADH4, S7 ribosomal protein) characters. Two sympatric species from Juan Fernández in the southeast Pacific are not sister taxa, but rather exhibit independent relationships to Australian/New Zealand chironemids. The most plausible explanation for these relationships and contemporary distributions is an Australian/New Zealand origin of the family, followed by two trans-Pacific dispersal and colonization events, facilitated by larval entrapment within the West Wind Drift. This study demonstrates that the diversity of taxa on an island can reflect multiple colonizations, rather than in situ diversification, even in the case of very small, isolated, and geologically recent islands. When taken in conjunction with studies of related taxa, our results indicate that transoceanic dispersal of temperate cirrhitoid fishes in the South Pacific has been frequent and unidirectional. Molecular estimates of divergence time between southeast Pacific chironemids and their western relatives predate the emergence of Juan Fernández, consistent with hypotheses that much of the marine nearshore faunas of young southeast Pacific islands may be the product of successive transfer from older, now submerged islands.
Keywords: Approximately unbiased test; biogeography; combinability; dispersal; island; seamount; Southern Hemisphere; West Wind Drift
Received November 21, 2004; Revised February 14, 2005; Accepted March 6, 2006
Geologically recent oceanic islands have been pivotal in the development and illustration of biogeographic and evolutionary theory (Darwin, 1859; MacArthur and Wilson, 1967; Emerson, 2002). Two such theories are that islands are colonized at a rate inversely proportional to their isolation (e.g., Diamond, 1972), and subsequent diversification is promoted by the availability of vacant niches and reduced competition and predation (Whittaker, 1998). If an island is sufficiently isolated and factors promoting the development of intraspecific divergence are in place, the rate at which new taxa arise on that island via in situ speciation may exceed that resulting from colonization, with notable examples comprising Darwin's finches on the Galápagos Islands (Sato et al., 2001) and silverswords and "picture winged" Drosophila of Hawaii (Carson and Kaneshiro, 1976; Baldwin, 1997). However, even at the most isolated of islands, multiple colonizations, rather than in situ speciation, may still explain the presence of related taxa (e.g., Gillespie et al., 1994; Howarth and Gardner, 1997; Emerson, 2002; Vences et al., 2003; Arensburger et al., 2004).
Whether the presence of related taxa on an island reflects in situ diversification or multiple colonizations can be reconciled via the reconstruction of phylogenetic relationships among island and mainland forms; if island taxa are monophyletic, a single colonization is favored, whereas paraphyly suggests multiple colonizations (although back colonization to the mainland may also be implicated; Emerson, 2002). Phylogeny reconstruction based on molecular characters has been employed to address this question (Emerson, 2002) and may be more successful than attempts based on morphological characters, particularly for taxa that have undergone limited morphological divergence or where morphological convergence may exist among island forms and obscure their true relationships (e.g., Rees et al., 2001; Cunha et al., 2005). The temporal scale of in situ diversification or colonization may also be estimated from the amount of molecular change (e.g., Baldwin and Sanderson, 1998; Sato et al., 2001).
The volcanic islands of the Juan Fernández and Desventuradas archipelagos occur approximately 600 km off the coast of Chile (Fig. 1). As with many isolated islands, a high degree of endemism is apparent in the marine flora and fauna of these archipelagos, 49%, 30%, and 26% for nearshore fishes, macroalgae, and molluscs, respectively (Bernard et al., 1991; Santelices, 1992; Pequeño and Lamilla, 2000; Pequeño and Sáez, 2000). However, more interesting than such high degrees of endemism per se are the young ages of these volcanic islands, probably no greater than 6 My old (Stuessy et al., 1984; Baker et al., 1987; González-Ferrán, 1987; Haase et al., 2000), and the much greater systematic affinities of their marine macroalgae and nearshore fishes with those of the Indo-West Pacific, particularly Australia and New Zealand, rather than those more proximate in South America (Santelices, 1992; Pequeño and Lamilla, 2000; Pequeño and Sáez, 2000). The western affinities of Juan Fernández and the Desventuradas marine taxa appear best explained by prevailing ocean currents, which offer direct (albeit long distance) dispersal from the southwest Pacific, but little opportunity for dispersal westward from Chile (Fig. 1; Santelices, 1992; Pequeño and Lamilla, 2000).
|
Chironemids (Perciformes: Chironemidae) are a group of marine nearshore fishes with representatives in the Juan Fernández and Desventuradas Islands and obvious systematic affinities with Australia and New Zealand. Two species occur sympatrically in the Juan Fernández Islands (Fig. 1): Chironemus bicornis (Steindachner, 1898) and C. delfini (Porter, 1914). The Desventuradas Islands to the north also host C. bicornis, but earlier reports of C. delfini (e.g., Pequeño and Lamilla, 2000) are erroneous (Dyer and Westneat, personal communication). The other members of this family comprise Threpterius maculosus Richardson, 1850, and C. georgianus Cuvier, 1829 from southern Australia; C. marmoratus Günther, 1860 from southeast Australia, Lord Howe Island, and northern New Zealand; and C. microlepis Waite, 1916 from the southwest Pacific islands of Lord Howe, Norfolk, and the Kermadecs (Fig. 1; Gomon et al., 1994; Francis, 1993, 2001). In the most recent revision of southeast Pacific chironemids, Meléndez (1990) noted that C. bicornis and C. delfini were more similar to Australian/New Zealand taxa than each other, albeit based solely on the presence or absence of supraorbital tubercles. If this character reflects phylogenetic relationships, the biogeographic history of this group would be remarkable, involving multiple trans-Pacific (> 8000 km) dispersal events and possibly independent colonization of the southeast Pacific islands.
The aim of this study was to reconstruct the phylogenetic relationships of chironemid species and interpret these relationships in a biogeographic context. Our null hypothesis is that the southeast Pacific chironemids are monophyletic, reflecting in situ diversification and a single colonization from the west. We surveyed morphology and mitochondrial and nuclear DNA (mtDNA, nDNA) characters to maximize the chances of recovering the species geneology (Wheeler et al., 1993). Comparatively slowly (16S ribosomal RNA; lrRNA) and rapidly (NADH dehydrogenase subunit 4; NADH4) evolving mtDNA regions were sequenced in an effort to gain sufficient phylogenetic signal to resolve chironemid relationships across a potential range of divergences. Among nDNA sequences the first and second introns of the S7 ribosomal protein (S7 RP) gene provide many characters, PCR priming sites appear widely conserved among fishes, and resultant data have demonstrated phylogenetic utility at a variety of taxonomic levels (Chow and Hazama, 1998; Chow et al., 2001; Wang et al., 2002; Lavoué et al., 2003; Page et al., 2003; Bernardi et al., 2004; Near et al., 2004; Teske et al., 2004). We also employed a molecular clock to assess the temporal scale of chironemid relationships, given previous suggestions that the comparatively high endemicity of young southeast Pacific island marine faunas may reflect ancient colonization of islands that have subsequently submerged, with successive faunal transfer to younger archipelagos (Springer, 1982; Newman and Foster, 1983).
|
Materials and Methods |
|---|
|
TopNotesAbstractMaterials and MethodsResultsDiscussionAcknowledgmentReferences |
|---|
Data Collection
Morphological and molecular data were collected for all chironemid species. A morphological dataset comprising 50 characters (28 osteological) was obtained from a taxonomic revision of the Chironemidae (Meléndez and Dyer, unpublished). Twenty-five characters were ordered (12 two-state, 13 three-state) and 25 unordered (14 two-state, nine three-state, two four-state). Sampling details of specimens for DNA sequence analysis are given in Figure 1. As the Chironemidae are thought to reside phylogenetically within an assemblage of perciforms known as the "cirrhitoids" (Nelson, 1994; Greenwood, 1995), representatives of the other families within this assemblage were employed as outgroups: Paracirrhites forsteri (Schneider) (Cirrhitidae), Chirodactylus variegatus (Valenciennes) (Latridae sensuBurridge and Smolenski, 2004), Aplodactylus punctatus Valenciennes (Aplodactylidae).
DNA extraction, PCR, and sequencing methods generally followed those of Burridge (2000) and Burridge and White (2000). We employed primers ND4LB (Bielawski and Gold, 2002) and NAP2 (Arevalo et al., 1994) to amplify 651 bp of NADH4, primers 16Sar-L and 16Sbr-H (Palumbi, 1991) for approximately 575 bp of lrRNA, and primers S7RPEX1F and S7RPEX3R (Chow and Hazama, 1998) for the first and second introns and second exon of S7 RP. "NAP2 modified" (5' AGC TTC TAC GTT GRG CTT TAG GGA G 3') was required to amplify NADH4 from C. georgianus. Annealing temperatures were 48, 55, and 60°C for NADH4, lrRNA, and S7RP, respectively. Both DNA strands were sequenced using ABI PRISM BigDye Terminator Cycle Sequencing. Intraindividual length variation in the first intron of S7 RP complicated the sequencing of several individuals, in which case PCR products were cloned using the pGEM-T Easy Vector system (Promega) prior to sequencing.
Phylogeny Reconstruction
DNA sequences were aligned visually and with reference to secondary structure models for lrRNA (De Rijk et al., 1998; Waters et al., 2000b). Homogeneity 
2 analyses were used to identify any significant difference in the nucleotide composition of variable sites among taxa, as sequences may be grouped on this basis rather than phylogenetic history (Lockhart et al., 1994; Tarrio et al., 2001; Jermiin et al., 2004). Given the tendency for saturation of transition nucleotide substitutions at third codon positions of mitochondrial protein-coding genes, we examined the relative accumulation of transitions (TI) and transversions (TV) during pairwise comparisons of taxa to assess saturation at these positions and employed different substitution weighting schemes accordingly.
When different groups of phylogenetically informative characters (data partitions) share the same evolutionary history and dynamics of character-state change, their combined analysis should increase the accuracy of phylogenetic inference; but if either of these factors varies among partitions, combined analysis may produce erroneous phylogenies (Bull et al., 1993; Huelsenbeck et al., 1996). The pairwise combinability of morphology, lrRNA, NADH4, and S7 RP partitions was assessed under the parsimony criterion using the incongruence length difference test (ILD; Farris et al., 1994, 1995), implemented by PAUP* (Swofford, 2004). Uninformative characters were excluded (Cunningham, 1997a, 1997b; Lee, 2001; Darlu and Lecointre, 2002), gaps were treated as missing data, and all character-state changes were equally weighted. One thousand permutations of characters among partitions were analyzed via branch and bound tree searches. Unfortunately, the ILD test can be biased under some circumstances (Graham et al., 1998; Dolphin et al., 2000; Barker and Lutzoni, 2002; Darlu and Lecointre, 2002; Dowton and Austin, 2002; Hipp et al., 2004), and correct phylogenies can be returned from combined partitions when combinability is rejected via the ILD test (Yoder et al., 2001; Barker and Lutzoni, 2002). Consequently, use of the ILD test as a single criterion for combinability could be misleading (Hipp et al., 2004).
We also assessed combinability under maximum likelihood based on whether topologies obtained for each DNA data partition could be rejected as plausible estimates of phylogeny by alternate partitions under the approximately unbiased test (AU test; Shimodaira, 2002). Firstly, the maximum likelihood topology for each DNA partition was recovered via heuristic searches (10 random sequence additions) using PAUP* and the most appropriate nucleotide substitution model selected for each partition by ModelTest 3.7 (hierarchical likelihood ratio test; Posada and Crandall, 1998). Secondly, for each DNA partition a large number of "short" trees were recovered via unweighted parsimony analysis using heuristic searches as above, but incrementally increasing the "KEEP" score above that of the minimum length topology until at least 2000 near-most-parsimonious trees were retained. These parsimony-generated "short" topology sets were supplemented with the maximum likelihood topologies from alternate DNA partitions if not already present. Thirdly, for each DNA partition the likelihood score of each nucleotide site in each "short" topology was calculated using PAUP* under the appropriate nucleotide substitution model, and the AU test was then performed using CONSEL 0.1f (Shimodaira and Hasegawa, 2001) to return a confidence set of topologies. Finally, the confidence set of each DNA partition was searched for the presence of maximum likelihood topologies from alternate partitions. If DNA partitions differ significantly in phylogenetic history, the maximum likelihood topology from one partition will not fall within the AU confidence set derived from another partition. The size of each confidence set also provides an indication of phylogenetic certainty provided by that partition.
Once the combinability of data partitions was determined, searches for optimum topologies were performed under maximum parsimony (DNA, morphology), maximum likelihood (DNA only), and Bayesian inference (DNA, morphology). Maximum parsimony analyses employed the branch and bound search algorithm with gaps treated as missing data. Maximum likelihood topologies were recovered by PAUP* using the most appropriate nucleotide substitution model across combinable partitions selected by ModelTest. Nonparametric bootstrap support (Felsenstein, 1985) was assessed using branch and bound searches under parsimony (2000 pseudoreplicate data sets), and heuristic searches with 10 random sequence additions under maximum likelihood (200 pseudoreplicate data sets). Groups compatible with the 50% majority-rule consensus were retained.
"Mixed model" Bayesian analysis of combinable partitions was conducted using MrBayes 3.0b4 (Ronquist and Huelsenbeck, 2003), employing the partition-specific models obtained from ModelTest for DNA data and a modified Markov model for morphological data (Lewis, 2001). Variable rates were allowed among partitions, and model parameters were drawn from the default prior probability distributions (see Ronquist and Huelsenbeck, 2003). Initially, four Metropolis-coupled Monte Carlo Markov chains (three heated according to Temp = 0.2) of 105 generations were run, starting from random trees and sampling topologies every 100 generations. Log-likelihood scores and estimates of model parameters were plotted to locate the attainment of stationarity, and trees from preceding generations were discarded as burn-in (Huelsenbeck et al., 2002). To reduce bias, this analysis was repeated to test stationarity values for convergence. If convergence was not attained among 105 generation chains, replicate chains of 106 generations were run instead. Entrapment in local optima was assessed by checking for convergence between shorter (105 to 106) and longer (106 to 107) generation runs (Huelsenbeck et al., 2002). Data subsequent to burn-in from convergent runs were used to estimate majority-rule consensus topologies and bipartition posterior probability.
Dispersal-Vicariance Analysis
Dispersal-vicariance analysis (DIVA; Ronquist, 1997) was performed to determine likely ancestral distributions, which is relevant to the reconstruction of biogeographic history. To minimize uncertainty around basal reconstructions (i.e., the ancestral distribution of the Chironemidae), the Aplodactylidae and Latridae (sensu Burridge and Smolenski, 2004) were incorporated into the analysis as outgroups, and the number of ancestral areas was limited to two (Ronquist, 1996). As the relationships among the Chironemidae, Aplodactylidae, and Latridae are uncertain (Burridge and Smolenski, 2004), DIVA was performed on the three possible rooted topologies among these families. The Aplodactylidae was represented by the two phylogenies recovered by Burridge (2000). As some relationships among latrids are uncertain (Burridge and Smolenski, 2004), a single terminal representing the entire family was employed, with an Australian–New Zealand ancestral distribution based on the "common equals primitive" criterion as recommended by Ronquist (1996). Contemporary distributions were scored as Australia, New Zealand, southwest Pacific islands (Lord Howe, Norfolk, Kermadecs), southeast Pacific islands (Juan Fernández, Desventuradas), and Chile.
Estimation of Divergence Times
Clock-like evolution of DNA sequences among chironemids was assessed via a likelihood-ratio test (Huelsenbeck and Crandall, 1997). We restricted our analysis to the chironemids, avoiding any non-clock-like evolution contributed by outgroups that is not relevant to our study. Given a lack of fossil or biogeographic information that could be employed to calibrate a molecular clock specifically for chironemids or their relatives, we employed a range of mitochondrial protein-coding gene calibrations derived for other fishes (1.66%/Mya, McKay et al., 1996; 1.3%/Mya, Bermingham et al., 1997; 1.52%/Mya, Zardoya and Doadrio, 1999; 0.84%/Mya, Perdices and Doadrio, 2001; 0.54%/Mya, Sivasundar et al., 2001; 1.31%/Mya, Dowling et al., 2002; 0.9%/Mya, Doadrio and Domínguez, 2004). These external calibrations are based on either fossils or well-characterized vicariance events, such as the uplift of Panama (Coates and Obando, 1996) or the Messinian salinity crisis (Krijgsman et al., 1999). Given that that first fossil appearance is likely to underestimate the age of a group and that genetic divergence may predate a vicariance event, these calibrations can be considered overestimates of the underlying divergence rate. In addition, most of the above calibrations were derived from corrected levels of sequence divergence, yet during this study we applied them to uncorrected NADH4 distances. Consequently, the application of these calibrations in this manner will provide an overly recent age of trans-Pacific chironemid divergence, and therefore conservative assessment of whether chironemids colonized the southeast Pacific after the emergence of Juan Fernández and the Desventuradas (our null hypothesis).
|
Results |
|---|
|
TopNotesAbstractMaterials and MethodsResultsDiscussionAcknowledgmentReferences |
|---|
Data Characteristics
All sequences are deposited in GenBank (DQ462667 [GenBank] to DQ462702 [GenBank] ). General details of variation in each data partition (informative characters, consistency index, selected nucleotide substitution model) are provided in Table 1. Length mutations and stop codons were absent among NADH4 and S7 RP exon 2 sequences. Inferred lrRNA secondary structures were consistent with published models. Consequently, orthology of DNA sequences is inferred among taxa (Zhang and Hewitt, 1996; Bensasson et al. 2001; but see Olson and Yoder, 2002). Heterogeneity of nucleotide composition at variable sites was absent from each DNA partition (P > 0.25). As most chironemids were similar in divergence from one another, it was not possible to identify any reduction in the observed rate of TI accumulation relative to TV accumulation at third codons of NADH4 with increasing levels of sequence divergence (not shown). However, exclusion of TI substitutions at NADH4 third codon positions during parsimony analysis had no impact on unrooted chironemid relationships and produced similar levels of bootstrap support (not shown).
|
" is the shape parameter of the gamma-distributed variation of rates among characters.Data Partition Combinability
With the inclusion of all taxa, pairwise combinability of the majority of DNA partitions was rejected based on the ILD test (Table 2). Exceptions were the comparisons of NADH4 with either lrRNA or S7 RP (Table 2). However, unweighted maximum parsimony topologies from each DNA partition differed only with respect to relationships among outgroups and placement of the root among the chironemids (Fig. 2), and their combinability was not rejected by the ILD test when outgroups were ignored (Table 2). Similarly, the combinability of morphology data with each DNA partition was rejected based on all taxa, but not when outgroups were excluded (Table 2). Maximum likelihood analysis and the AU test recovered confidence sets of 1168, 63, and 21 topologies for lrRNA, NADH4, and S7 RP data partitions, respectively. The lrRNA data partition did not reject the maximum likelihood topologies from alternate DNA data partitions (Table 3). The NADH4 and S7 RP data partitions rejected the maximum likelihood lrRNA topologies, but not the maximum likelihood topologies obtained from each other (Table 3).
|
|
|
Given the above results, we suggest that the data partitions are combinable. Although the ILD test suggested incombinability for the majority of partitions during parsimony analysis of all taxa, combinability was not rejected when restricting analysis to the taxa of interest (the ingroup). The suggestion of incombinability by the ILD test with the inclusion of outgroups may reflect different levels of homoplasy among partitions at deeper phylogenetic levels (Graham et al., 1998; Dolphin et al., 2000; Barker and Lutzoni, 2002; Darlu and Lecointre, 2002), which are not of concern as long as they do not impact root placement within a combined analysis. To test the latter, alternate outgroup relationships and inclusion were enforced during combined parsimony analysis (see below). The AU test results are consistent with all three DNA partitions having experienced the same phylogenetic history; the NADH4 and S7 RP maximum likelihood topologies were present in each other's confidence set, and although the lrRNA maximum likelihood topologies were not in the S7 RP or NADH4 confidence sets, the lrRNA confidence set was very large and encompassed the S7 RP and NADH4 maximum likelihood topologies. Despite the lower phylogenetic certainty provided by lrRNA (i.e., large confidence set), its phylogenetic signal is consistent with that expressed by NADH4 or S7 RP, and hence may contribute to the recovery of the underlying evolutionary history during combined analysis.
Combined DNA Analysis
Maximum parsimony, maximum likelihood, and Bayesian inference analyses of combined partitions provided high support for the same set of chironemid relationships (Fig. 3). Neither the southeast Pacific (SEP) nor the Australia/New Zealand/southwest Pacific chironemids were clustered as monophyletic (Fig. 3). Instead, C. delfini from the SEP was placed as sister to C. georgianus from Australia, and C. bicornis from the SEP was placed as sister to a clade comprising Australia/New Zealand/southwest Pacific island taxa (C. marmoratus, C. microlepis) (Fig. 3). Root placement was identical in all analyses, but outgroup relationships differed in Bayesian analysis relative to maximum parsimony and likelihood, although corresponding topological support was low (Fig. 3). To assess whether root placement may have been impacted by the combined analysis of data partitions that are potentially incongruent at deeper phylogenetic levels (i.e., the significant ILD test results when including outgroups), alternate outgroup relationships and inclusion were enforced during combined parsimony analysis. However, the same set of rooted ingroup relationships and similar levels of topological support were recovered.
|
Dispersal-Vicariance Analysis (DIVA)
DIVA inferred an exclusively Australian ancestral distribution for the Chironemidae based on two of the three possible relationships among cirrhitoid families tested (Chironemidae sister to either the Aplodactylidae or Latridae). When the Chironemidae were assumed as sister to [Aplodactylidae + Latridae], Juan Fernández/Desventuradas archipelagos and Australian ancestral distributions were considered equally most likely.
Divergence Times
Likelihood scores for the NADH4 chironemid topology, either with or without the enforcement of a molecular clock, were not significantly different (72 = 9.98, P = 0.125). Consequently, NADH4 branch lengths derived from the enforcement of a molecular clock were employed for the estimation of chironemid divergence times. As we were primarily interested in whether trans-Pacific divergences may predate the emergence of both the Juan Fernández and Desventuradas archipelagos, we employed uncorrected (i.e., underestimated) sequence distances to provide overly recent estimates of divergence times. Chironemus delfini and C. bicornis were 22.0% and 13.6% divergent from their respective western relatives. Employing seven mitochondrial protein-coding gene calibrations derived from other fishes (0.54%/Mya to 1.66%/Mya), which in turn probably represent overestimates of actual divergence rates given their derivations, yields trans-Pacific divergence time estimates of 13.2 to 40.8 and 8.2 to 25.2 Mya for C. delfini and C. bicornis, respectively.
|
Discussion |
|---|
|
TopNotesAbstractMaterials and MethodsResultsDiscussionAcknowledgmentReferences |
|---|
Multiple trans-Pacific Dispersals
Analysis of combinable data partitions (50 morphological characters and 2251 characters from three DNA regions) did not recover the southeast Pacific (SEP) chironemids as monophyletic. Instead, C. delfini from the SEP was placed as sister to C. georgianus from Australia, and C. bicornis from the SEP was placed as sister to a clade comprising Australia/New Zealand/southwest Pacific island taxa (C. marmoratus, C. microlepis). Consequently, on the basis of independent western affinities of SEP chironemids, we invoke multiple trans-Pacific dispersal and colonization events for the contemporary distribution of the family. However, this does not necessarily implicate independent colonizations of the SEP islands; the family may have originated and continually maintained a presence in SEP such that in situ diversification explains C. bicornis and C. delfini, whereas all contemporary Australian/New Zealand/southwest Pacific forms reflect multiple westward dispersals. Hence, the important question becomes "Where did the family originate?"
Independent Colonizations of the Southeast Pacific
We favor an Australian/New Zealand origin of chironemids and multiple colonizations of the SEP for several reasons. Firstly, under the grounds of parsimony, only two trans-Pacific dispersal events are required to explain the contemporary distribution of chironemids under a "western ancestry, multiple colonizations of the SEP" scenario, whereas three trans-Pacific dispersal events are required for a "SEP ancestry and in situ diversification" scenario (Fig. 4). Although parsimony reconstructions accommodating costs for sympatric speciation, vicariance, and extinction in addition to dispersal (Cook and Crisp, 2005: Equation 1) cannot favor one chironemid biogeographic scenario over the other, assuming greater cost for eastward relative to westward dispersal, consistent with contemporary oceanographic conditions (see below), favors a western origin and multiple eastward dispersals.
|
The fact that Australian and New Zealand chironemids occupy landmasses of long geological history, whereas the SEP chironemids occupy recent volcanic islands (< 6 My old; Stuessy et al., 1984; Baker et al., 1987; González-Ferrán, 1987; Haase et al., 2000), also supports a western ancestry and multiple eastward dispersals (Cook and Crisp, 2005). In addition, DIVA inferred an Australian ancestral distribution for the Chironemidae under all three of the possible relationships among cirrhitoid families tested, and only under one of these relationships (Chironemidae sister to [Aplodactylidae + Latridae]) was a Juan Fernández/Desventuradas Islands origin considered equally likely to that of Australia.
With respect to oceanography, westward trans-Pacific dispersal by chironemids would be more difficult than eastward dispersal. The South Equatorial Current is comparatively slow (< 0.1 ms–1) in all but the central Pacific (Lukas, 2001), which would equate to a South Pacific transit time in excess of 900 days. Use of the South Equatorial Current by temperate fishes would also require larvae tolerant of tropical temperatures (< 20°S; Fig. 1). In contrast, eastward dispersal from Australia/New Zealand via the West Wind Drift appears more feasible in terms of current speed and temperature, and has been widely invoked for many other similarly distributed taxa (Fell, 1962; Newman, 1979; Briggs, 1974:126, 1995:251; McDowall, 1978; Santelices, 1992; Beu et al., 1997; Burridge, 1999, 2000; Ó Foighil et al., 1999, Waters et al., 2000a; Thiel, 2002; Williams et al., 2003; Donald et al., 2005). Although little is known of the early life history of chironemid fishes (Neira et al., 1998), they may share the open-water, 7- to 12-month pelagic larval stage exhibited by their close cirrhitoid relatives (e.g., Annala, 1987; Andrew et al., 1995), which presumably enabled these groups to colonise many isolated islands and form transoceanic disjunctions (Burridge, 1999, 2000; Burridge and White, 2000; Burridge and Smolenski, 2004). Although adult and juvenile chironemids occupy nearshore habitats, a recent observation indicates that these life history stages could potentially "raft" with drifting objects (Dempster and Kingsford, 2004), representing another possible means of transoceanic dispersal. Kelp rafts are particularly abundant in the southern Ocean and represent a plausible vector for such dispersal (Smith, 2002; Donald et al., 2005).
Consequently, our study demonstrates that the diversity of island forms can reflect multiple colonizations, rather than in situ diversification, even in the case of very small, isolated, and geologically recent islands. The results of this study, in combination with others (Gillespie et al., 1994; Howarth and Gardner, 1997; Emerson, 2002; Arensburger et al., 2004), indicate that the presence of related taxa on isolated or recent islands should not be construed as examples of in situ diversification in the absence of reliable phylogenetic analysis. Likewise, this study demonstrates that the frequency of transoceanic dispersal and colonization is likely to be underestimated based on the assessment of species distributions alone, even in cases where oceanic dispersal was known or suspected for a group (e.g., by the occupation of oceanic islands; de Queiroz, 2005).
Nonrandom Dispersal across the Pacific
The results of this study add to a body of molecular-based evidence for recent dispersal of temperate cirrhitoid fishes from Australia/New Zealand to the SEP. Both Nemadactylus (Latridae, sensuBurridge and Smolenski, 2004) and Aplodactylus (Aplodactylidae) are predominantly Australian/New Zealand in distribution, but have recent derivatives in the SEP. Nemadactylus gayi at Juan Fernández, the Desventuradas, and proximate seamounts is the sister taxon of Nemadactylus sp. in Australia/New Zealand (Burridge, 1999), whereas A. punctatus occurs along the west coast of South America and its sister taxon is A. arctidens from Australia/New Zealand (Burridge, 2000). Nemadactylus bergi, more commonly known from the east coast of South America but recently reported from the SEP (Nakamura, 1986; Pequeño, 2004), may represent an additional eastward trans-Pacific dispersal within Nemadactylus. Similarly, if the tentative sister-taxon relationship of Cheilodactylus spectabilis (Australia/New Zealand) and Chirodactylus variegatus (west coast of South America) (Burridge and Smolenski, 2004) was confirmed, it would likely represent another eastward trans-Pacific dispersal by cirrhitoid fishes.
The presence of concordant cirrhitoid biogeographic histories involving eastward dispersal across the Pacific, in addition to those proposed for other taxa (Fell, 1962; Newman, 1979; Briggs, 1974:126, 1995:251; McDowall, 1978; Santelices, 1992; Beu et al., 1997; Parin et al., 1997; Ó Foighil et al., 1999; Waters et al., 2000a; Thiel, 2002; Williams et al., 2003; Donald et al., 2005) supports McDowall's (2004) assertion that "some dispersal events may be surprisingly regular and enduring in source, direction and target area," refuting positions of Croizat et al. (1974) and Craw (1979) that dispersal is random and cannot be responsible for congruent or concordant patterns among different taxa. Sanmartín and Ronquist (2004) also provided evidence of congruent dispersal among elements of the Southern Hemisphere flora. Our cirrhitoid observations also support Cook and Crisp's (2005) hypothesis that if congruent directional dispersal and successful colonization is observed across unrelated taxa, then it should also be possible in related taxa.
Evidence for Ancient Archipelagos?
Despite the potential errors that can be associated with the application of external molecular clock calibrations (Rand, 1994), the underlying nature of the seven calibrations employed herein, and the manner in which we applied them, are likely to yield underestimates of trans-Pacific chironemid divergence time (see Materials and Methods). However, the estimated divergence times of Juan Fernández and Desventuradas chironemids from their closest relatives predate the ages of these SEP islands. Divergence times of C. delfini and C. bicornis from their closest relatives were 13.2 to 40.8 and 8.2 to 25.2 Mya, respectively. In contrast, K-Ar dating indicates that most members of the Juan Fernández and Desventuradas archipelagos are less than 4.5 My old (Stuessy et al., 1984; Baker et al., 1987; González-Ferrán, 1987; Haase et al., 2000). Santa Clara, within the Juan Fernández islands, may be slightly older, but has a large uncertainty surrounding its age due to correction for atmospheric 40Ar (5.8 ± 2.1 My; Stuessy et al. 1984). Similar results were derived for Austrolittorina, a group of nearshore gastropods in which the Juan Fernández representative apparently diverged from its southern Australian sister taxon 13 to 30 Mya (Williams et al., 2003). Both chironemid and Austrolittorina estimates of divergence time also correspond to an intensive period of trans-Pacific dispersal evident from the molluscan fossil record, perhaps correlated to increased current flow during cooler climates (Beu et al., 1997).
Our molecular clock results are consistent with previous suggestions that much of the marine nearshore faunas of young SEP islands may be the product of successive transfer from older, now submerged islands (Springer, 1982; Newman and Foster, 1983). This hypothesis was developed to explain the comparatively high endemicity of nearshore taxa at young and small SEP islands. For example, species endemicity of the marine mollusc fauna at Easter Island (
2 My old) is estimated at 42%, in contrast to that for the Hawaiian chain (at least 20 My old), which is approximately 20% (Newman and Foster, 1983). Reconstructions of Nazca Plate movement and depth indicate that even an incomplete sample of seamounts along the Sala y Gómez and Nazca ridges provides a chronological continuity of emergent islands throughout the last 34 My (Fig. 5; Newman and Foster, 1983; see also Parin et al., 1997); these islands were produced by a mantle plume presently located near Sala y Gómez (O'Conner et al., 1995). Chironemids may have initially colonized these previously emergent islands and were subsequently transferred to the Juan Fernández and Desventuradas archipelagos. The distribution of a deeper water cirrhitoid is consistent with this hypothesis; Nemadactylus gayi presently inhabits Juan Fernández, the Desventuradas, and at least one seamount of the Nazca ridge (Parin, 1991; Pequeño and Lamilla, 2000).
|
Alternatively, and as suggested for Austrolittorina by Williams et al. (2003), dispersal from Australia/New Zealand to Juan Fernández and the Desventuradas may have proceeded by geographically intermediate stepping stones. Seamount faunas in places such as the Foundation chain (Fig. 5) are poorly characterized, but recent surveys in this region have detected populations that may link the Australian/New Zealand demersal marine fauna with those further east (e.g., Jasus caveorum, Webber and Booth, 1995; Polyprion oxygeneios, Latris spp., Roberts, 2003). The ages of these seamounts also span at least the last 21 My (O'Conner et al., 1998), and some were undoubtedly emergent during the past (Devey et al., 1995). We consider it unlikely that both SEP chironemid species could represent recent (< 8 Mya) trans-Pacific dispersal events from lineages of Australian/New Zealand chironemids that subsequently left no contemporary descendants in that region. Colonization of insular environments is noted as a dominant initiator of cladogenesis (Waters and Wallis, 2001; Emerson, 2002; Donald et al., 2005), and all but one node in the chironemid species phylogeny can be ascribed to island colonization (Fig. 4).
|
Acknowledgment |
|---|
|
TopNotesAbstractMaterials and MethodsResultsDiscussionAcknowledgmentReferences |
|---|
FONDECYT Chile grant no. 1990172 supported this project. The following individuals are thanked for the provision of specimens and tissue samples for genetic analysis: J. Clarke (Smallcraft, Two Rocks, Western Australia), J. Fariña and P. Ojeda (Pontificia Universidad Catolica de Chile), M. McGrouther (Australian Museum), A. Stewart (Museum of New Zealand), K. Truong (Deakin University), M. Westneat (Field Museum, Chicago). Drs. B. Emerson, R. McDowall, R. Page, A. Patterson, S. Trewick, and J. Waters provided comments that improved the manuscript, along with members of the Molecular Ecology and Biodiversity Laboratory, Deakin University.
|
Notes |
|---|
|
TopNotesAbstractMaterials and MethodsResultsDiscussionAcknowledgmentReferences |
|---|
4 Current Address: Department of Zoology, University of Otago, 340 Great King Street, Dunedin, New Zealand E-mail: Chris.Burridge{at}stonebow.otago.ac.nz (C.P.B.)
|
References |
|---|
|
TopNotesAbstractMaterials and MethodsResultsDiscussionAcknowledgmentReferences |
|---|
-
Andrew T. G., Hecht T., Heemstra P. C., Lutjeharms J. R. E. Fishes of the Tristan da Cunha group and Gough Island, South Atlantic Ocean. Ichthyol. Bull. J. L. B. Smith Inst. Ichthyol. (1995) 63:459–468.
Annala J. H. The biology and fishery of tarakihi, Nemadactylus macropterus, in New Zealand waters. N. Z. Fish. Res. Div. Occ. Pub. (1987) 51:459–468.
Arensburger P., Buckley T. R., Simon C., Moulds M., Holsinger K. E. Biogeography and phylogeography of the New Zealand cicada genera (Hemiptera: Cicadidae) based on nuclear and mitochondrial DNA data. J. Biogeogr. (2004) 31:459–468.
Arevalo E., Davis S. K., Sites J. W. Mitochondrial DNA sequence divergence and phylogenetic relationships among eight chromosome races of Sceloporus grammicus complex (Phrynosomatidae) in central Mexico. Syst. Biol. (1994) 43:459–468.
Baker P. E., Gledhill A., Harvey P. K., Hawkesworth C. J. Geochemical evolution of the Juan Fernández Islands, SE Pacific. J. Geol. Soc. Lond. (1987) 144:459–468.
Baker R. H., DeSalle R. Multiple sources of character information and the phylogeny of Hawaiian drosophilids. Syst. Biol. (1997) 46:459–468.
Baldwin B. G. Adaptive radiation of the Hawaiian silversword alliance: Congruence and conflict of phylogenetic evidence from molecular and non-molecular investigations. In: Molecular evolution and adaptive radiation—Givnish T. J., Sytsma K. J., eds. (1997) UK: Cambridge University Press. 103–128.
Baldwin B. G., Sanderson M. J. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl. Acad. Sci. USA (1998) 95:459–468.
Barker K. H., Lutzoni F. M. The utility of the incongruence length difference test. Syst. Biol. (2002) 51:459–468.
Bensasson D., Zhang D. -X., Hartl D. L., Hewitt G. M. Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends Ecol. Evol. (2001) 16:459–468.
Bernard F. R., McKinnell S. M., Jamieson G. S. Distribution and zoogeography of the Bivalvia of the eastern Pacific Ocean. Can. Spec. Publ. Fish. Aquat. Sci. (1991) 112:459–468.
Bermingham E., McCafferty S. S., Martin A. P. Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus. In: Molecular systematics of fishes—Kocher T. D., Stepien C. A., eds. (1997) San Diego: Academic Press. 113–128.
Beu A. G., Griffin M., Maxwell P. A. Opening of Drake Passage gateway and Late Miocene to Pleistocene cooling reflected in Southern Ocean molluscan dispersal: evidence from New Zealand and Argentina. Tectonophysics (1997) 281:459–468.
Bielawski J. P., Gold J. R. Mutation patterns of mitochondrial H- and L-strand DNA in closely related cyprinid fishes. Genetics (2002) 161:459–468.
Briggs J. C. Marine zoogeography (1974) New York: McGraw-Hill.
Briggs J. C. Global biogeography (1995) Amsterdam: Elsevier.
Bull J. J., Huelsenbeck J. P., Cunningham C. W., Swofford D. L., Waddell P. J. Partitioning and combining data in phylogenetic analysis. Syst. Biol. (1993) 42:459–468.
Burridge C. P. Molecular phylogeny of Nemadactylus and Acantholatris (Perciformes: Cirrhitoidea: Cheilodactylidae), with implications for taxonomy and biogeography. Mol. Phylogenet. Evol. (1999) 13:93–109.[CrossRef][Web of Science][Medline]
Burridge C. P. Molecular phylogeny of the Aplodactylidae (Perciformes: Cirrhitoidea), a group of Southern Hemisphere marine fishes. J. Nat. Hist. (2000) 34:459–468.
Burridge C. P., Smolenski A. J. Molecular phylogeny of the Cheilodactylidae and Latridae (Perciformes: Cirrhitoidea) with notes on taxonomy and biogeography. Mol. Phylogenet. Evol. (2004) 30:459–468.
Burridge C. P., White R. W. G. Molecular phylogeny of the antitropical subgenus Goniistius (Perciformes: Cheilodactylidae: Cheilodactylus): Evidence for multiple transequatorial divergences and non-monophyly. Biol. J. Linn. Soc. (2000) 70:459–468.[CrossRef][Web of Science]
Carson H. L., Kaneshiro K. Y. Drosophila of Hawaii: Systematics and evolutionary genetics. Ann. Rev. Ecol. Syst. (1976) 7:311–345.[CrossRef][Web of Science]
Chow S., Hazama K. Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol. Ecol. (1998) 7:459–468.
Chow S., Scholey V. P., Nakazawa A., Margulies D., Wexler J. B., Olson R. J., Hazama K. Direct evidence for Mendelian inheritance of the variations in the ribosomal protein gene introns in yellowfin tuna (Thunnus albacares). Mar. Biotech. (2001) 3:459–468.
Coates A. G., Obando J. A. The geological evolution of the Central American Isthmus. In: Evolution and environment of tropical America—Jackson J., Budd A. F., Coates A. G., eds. (1996) Chicago: University of Chicago Press. 21–56.
Craw R. C. Generalised tracks and dispersal in biogeography: A response to R. M. McDowall. Syst. Zool. (1979) 28:459–468.
Croizat L., Nelson G., Rosen D. E. Centres of origin and related concepts. Syst. Zool. (1974) 23:459–468.
Cunha R. L., Castilho R., Rüber L., Zardoya R. Patterns of cladogenesis in the venomous marine gastropod genus Conus from the Cape Verde Islands. Syst. Biol. (2005) 54:634–650.
Cunningham C. W. Is congruence between data partitions a reliable predictor of phylogenetic accuracy? Empirically testing an iterative procedure for choosing among phylogenetic methods. Syst. Biol. (1997a) 46:459–468.
Cunningham C. W. Can three incongruence tests predict when data should be combined? Mol. Biol. Evol. (1997b) 14:459–468.
Darlu P., Lecointre G. When does the incongruence length difference test fail? Mol. Biol. Evol. (2002) 19:459–468.
Darwin C. On the origin of species by means of natural selection (1859) London: J. Murray.
Dempster T., Kingsford M. J. Drifting objects as habitat for pelagic juvenile fish off New South Wales, Australia. Mar. Freshw. Res. (2004) 55:459–468.
De Rijk P., Caers A., Van de Peer Y., de Wachter R. Database on the structure of large ribosomal subunit RNA. Nucleic. Acids Res. (1998) 26:459–468.
Devey C. W., Hékinian R., Ackermand D., Binard N., Francke B., Hémond C., Kapsimalis V., Lorenc S., Maia M., Möller H., Perrot K., Pracht J., Rogers T., Stattegger K., Steinke S., Victor P. The Foundation Seamount chain: a first survey and sampling. Mar. Geol. (1995) 137:459–468.
Diamond J. M. Biogeographic kinetics: estimation of relaxation times for avifaunas of South-west Pacific islands. Proc. Natl. Acad. Sci. USA (1972) 69:459–468.
Doadrio I., Domínguez O. Phylogenetic relationships within the fish family Goodeidae based on cytochrome b sequence data. Mol. Phylogenet. Evol. (2004) 31:459–468.
Dolphin K., Belshaw R., Orme C. D. L., Quicke D. L. J. Noise and incongruence: interpreting results of the incongruence length difference test. Mol. Phylogenet. Evol. (2000) 17:459–468.
Donald K. M., Kennedy M., Spencer H. G. Cladogenesis as the result of long-distance rafting events in South Pacific topshells (Gastropoda, Trochidae). Evolution (2005) 59:459–468.
Dowling T. E., Tibbets C. A., Minckley W. L., Smith G. R. Evolutionary relationships of the plagopterins (Teleostei: Cyprinidae) from cytochrome b sequences. Copeia (2002) 2002:459–468.
Dowton M., Austin A. D. Increased congruence does not necessarily indicate increased phylogenetic accuracy—the behaviour of the incongruence length difference test in mixed-model analysis. Syst. Biol. (2002) 51:459–468.
Emerson B. C. Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol. Ecol. (2002) 11:459–468.
Farris J. S., Källersjö M., Kluge A. G., Bult C. Testing significance of incongruence. Cladistics (1994) 10:459–468.
Farris J. S., Källersjö M., Kluge A. G., Bult C. Constructing a significance test for incongruence. Syst. Biol. (1995) 44:459–468.
Fell H. B. West-wind-drift dispersal of echinoderms in the Southern Hemisphere. Nature (1962) 193:459–468.[CrossRef][Medline]
Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution (1985) 39:459–468.
Francis M. P. Checklist of the coastal fishes of Lord Howe, Norfolk, and Kermadec Islands, Southwest Pacific Ocean. Pac. Sci. (1993) 47:459–468.
Francis M. P. Coastal fishes of New Zealand (2001) Auckland: Reed Books.
Gillespie R. G., Croom H. B., Palumbi S. R. Multiple origins of a spider radiation in Hawaii. Proc. Natl. Acad. Sci. USA (1994) 91:459–468.
Gomon M. F., Glover J. C. M., Kuiter R. H. Fishes of Australia's south coast (1994) Adelaide: State Press.
González-Ferrán O. Evolución geológica de las islas chilenas en el Océano Pacífico. In: Islas oceánicas Chilenas: conocimiento científico y necesidades de investigaciones—Castilla J. C., ed. (1987) Santiago: Ediciones Universidad Católica de Chile. 37–54.
Graham S. W., Kohn J. R., Morton B. R., Moeckenwalder J. E., Barrett S. C. H. Phylogenetic congruence and discordance among one morphological and three molecular data sets from Pontederiaceae. Syst. Biol. (1998) 47:459–468.
Greenwood P. H. A revised familial classification for certain cirrhitoid genera (Teleostei, Percoidei, Cirrhitoidea), with comments on the group's monophyly and taxonomic ranking. Bull. Nat. Hist. Mus. Lond. (1995) 61:459–468.
Haase K. M., Mertz D. F., Sharp W. S., Garbe-Schonberg C. D. Sr-Nd-Pb isotope ratios, geochemical compositions, and Ar-40/Ar-39 data of lavas from San Felix Island (Southeast Pacific): Implications for magma genesis and sources. Terra Nova (2000) 1290–1296.
Hipp A. L., Hall J. C., Sytsma K. J. Congruence versus phylogenetic accuracy: revisiting the incongruence length difference test. Syst. Biol. (2004) 53:459–468.
Howarth D. G., Gardner D. E. Phylogeny of Rubus subgenus Idaeobatus (Rosaceae) and its implications toward colonisation of the Hawaiian Islands. Syst. Biol. (1997) 22:459–468.
Huelsenbeck J. P., Bull J. J., Cunningham C. W. Combining data in phylogenetic analysis. Trends Ecol. Evol. (1996) 11:459–468.
Huelsenbeck J. P., Crandall K. A. Phylogeny estimation and hypothesis testing using maximum likelihood. Ann. Rev. Ecol. Syst. (1997) 28:459–468.
Huelsenbeck J. P., Larget B., Miller R. E., Ronquist F. Potential applications and pitfalls of Bayesian inference of phylogeny. Syst. Biol. (2002) 51:459–468.
Jermiin L. S., Ho S. Y. W., Ababneh F., Robinson J., Larkum A. W. D. The biasing effect of compositional heterogeneity on phylogenetic estimates may be underestimated. Syst. Biol. (2004) 53:459–468.
Krijgsman W., Hilgen F. J., Raffi I., Sierro F. J., Wilson D. S. Chronology, causes and progression of the Messinian salinity crisis. Nature (1999) 400:459–468.
Last P. R., Scott E. O. G., Talbot F. H. Fishes of Tasmania (1983) Hobart: Tasmanian Fisheries Development Authority.
Lavoué S., Sullivan J. P., Hopkins C. D. Phylogenetic utility of the first two introns of the S7 ribosomal protein gene in African electric fishes (Mormyroidea: Teleostei) and congruence with other molecular markers. Biol. J. Linn. Soc. (2003) 78:459–468.
Lee M. S. Y. Uninformative characters and apparent conflict between molecules and morphology. Mol. Biol. Evol. (2001) 18:459–468.
Lewis P. O. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. (2001) 50:459–468.
Lockhart P. J., Steel M. A., Hendy M. D., Penny D. Recovering evolutionary trees under a more realistic model of sequence evolution. Mol. Biol. Evol. (1994) 11:459–468.[Abstract]
Lukas R. Pacific Ocean equatorial currents. In: Encyclopedia of ocean sciences—Steele J. H., Thorpe S. A., Turekian K. K., eds. (2001) San Diego: Academic Press. 2069–2076.
MacArthur R. H., Wilson E. O. The theory of island biogeography (1967) New Jersey: Princeton University Press, Princeton.
McDowall R. M. Generalised tracks and dispersal in biogeography. Syst. Zool. (1978) 27:459–468.
McDowall R. M. What biogeography is: a place for process. J. Biogeogr. (2004) 31:459–468.
McKay S. J., Devlin R. H., Smith M. J. Phylogeny of Pacific salmon and trout based on growth hormone type-2 and mitochondrial NADH dehydrogenase subunit 3 DNA sequences. Can. J. Fish. Aquat. Sci. (1996) 53:459–468.
Meléndez C. R. Chironemid fishes from Juan Fernández archipelago and Desventuradas Islands, Chile (Perciformes: Chironemidae). Rev. Biol. Mar. (1990) 25:459–468.
Nakamura I. Important trawled fishes off Patagonia (1986) Tokyo: Japan Marine Fishery Resource Research Center.
Near T. J., Bolnick D. I., Wainright P. C. Investigating phylogenetic relationships of sunfishes and black basses (Actinopterygii: Centrarchidae) using DNA sequences from mitochondrial and nuclear genes. Mol. Phylogenet. Evol. (2004) 32:459–468.
Nelson J. S. Fishes of the World (1994) New York: J. Wiley.
Neira F. J., Miskiewicz A. G., Rissik D. Chironemidae: kelpfishes. In: Larvae of temperate Australian fishes—Neira F. J., Miskiewicz A. G., Trnski T., eds. (1998) Nedlands, Western Australia: University of Western Australia Press. 215–217.
Newman W. A. On the biogeography of balanomorph barnacles of the southern Ocean including new balanid taxa; a subfamily, two genera and three species. (1979) Proceedings of the international symposium on marine biogeography and evolution in the Southern Hemisphere. Wellington: New Zealand Department of Scientific and Industrial Research. 279–306.
Newman W. A., Foster B. A. The Rapanuian faunal district (Easter and Sala y Gómez): in search of ancient archipelagos. Bull. Mar. Sci. (1983) 33:459–468.
O'Conner J. M., Stoffers P., McWilliams M. O. Time-space mapping of Easter Chain volcanism. Earth Planet. Sci. Lett. (1995) 136:459–468.
O'Connor J. M., Stoffers P., Wijbrans J. R. Migration rate of volcanism along the Foundation chain, SE Pacific. Earth Planet. Sci. Lett. (1998) 164:459–468.
O'Foighil D., Marshall B. A., Hilbish T. J., Pino M. A. Trans-Pacific range extension by rafting is inferred for the flat oyster Ostrea chilensis. Biol. Bull. (1990) 196:459–468.
Olson L. E., Yoder A. D. Using secondary structure to identify ribosomal numts: cautionary examples from the human genome. Mol. Biol. Evol. (2002) 19:459–468.
Page L. M., Hardman M., Near T. J. Phylogenetic relationships of barcheek darters (Percidae: Etheostoma, subgenus Catonotus) with descriptions of two new species. Copeia (2003) 2003:459–468.
Palumbi S. R., Martin A. P., Romano S., McMillan W. O., Stice L., Grabowski G. The simple fool's guide to PCR (1991) University of Hawaii. version 2.0.
Parin N. V. Fish fauna of the Nazca and Sala y Gómez submarine ridges, the easternmost outpost of the Indo-West Pacific zoogeographic region. Bull. Mar. Sci. (1991) 49:671–683.
Parin N. V., Mironov A. N., Nesis K. N. Biology of the Nazca and Sala y Gómez submarine ridges, an outpost of the Indo-West Pacific fauna in the eastern Pacific Ocean: composition and distribution of the fauna, its communities and history. Adv. Mar. Biol. (1997) 32:459–468.
Perdices A., Doadrio I. The molecular systematics and biogeography of the European cobitids based on mitochondrial DNA sequences. Mol. Phylogenet. Evol. (2001) 19:459–468.
Pequeño G. Nemadactylus bergi (Norman, 1937) frente a bahía mansa, Chile (Osteichthyes: Cheilodactylidae). Cienc. Tecnol. Mar. (2004) 27:121–125.
Pequeño G., Lamilla J. The littoral fish assemblage of the Desventuradas Islands (Chile) has zoogeographical affinities with the Western Pacific. Global Ecol. Biogeogr. (2000) 9:459–468.
Pequeño G., Sáez S. Los peces litorales del archipiélago de Juan Fernández (Chile): endemismo y relaciones ictiogeográficas. Invest. Mar. (2000) 28:27–37.
Posada D., Crandall K. A. ModelTest: testing the model of DNA substitution. Bioinformatics (1998) 14:459–468.
Rand D. M. Thermal habit, metabolic rate and the evolution of mitochondrial DNA. Trends Ecol. Evol. (1994) 9:125–131.[CrossRef]
Rees D. J., Emerson B. C., Oromí P., Hewitt G. M. The diversification of the genus Nesotes (Coleoptera: Tenebrionidae) in the Canary Islands: evidence from mtDNA. Mol. Phylogenet. Evol. (2001) 21:459–468.
Roberts C. D. A new species of trumpeter (Teleostei; Percomorpha; Latridae) from the central South Pacific Ocean, with a taxonomic review of the striped trumpeter Latris lineata. J. Roy. Soc. N. Z. (2003) 33:731–754.
Ronquist F. Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Syst. Biol. (1997) 46:195–203.
Ronquist F., Huelsenbeck J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (2003) 19:459–468.
Sanmartín I., Ronquist F. Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns. Syst. Biol. (2004) 53:459–468.
Santelices B. Marine phytogeography of the Juan Fernandez Archipelago: A new assessment. Pac. Sci. (1992) 46:438–452.
Sato A., Tichy H., O'hUigin C., Grant P. R., Grant B. R., Klein J. On the origin of Darwin's finches. Mol. Biol. Evol. (2001) 18:459–468.
Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. (2002) 51:492–508.
Shimodaira H., Hasegawa M. CONSEL: For assessing the confidence of phylogenetic tree selection. Bioinformatics (2001) 17:459–468.
Sivasundar A., Bermingham E., Ortí G. Population structure and biogeography of migratory freshwater fishes (Prochilodus: Characiformes) in major South American rivers. Mol. Ecol. (2001) 10:407–417.[CrossRef][Medline]
Smith S. D. A. Kelp rafts in the Southern Ocean. Global Ecol. Biogeog. (2002) 11:67–69.[CrossRef]
Springer V. G. Pacific Plate biogeography with special reference to shore fishes. Smith. Contr. Zool. (1982) 367:1–182.
Stuessy T. F., Foland K. A., Sutter J. F., Sanders R. W., Silva M. Botanical and geological significance of potassium-argon dates from the Juan Fernández Islands. Science (1984) 225:459–468.
Swofford D. L. PAUP*. Phylogenetic analysis using parsimony (*and other methods) (2004) Sunderland, Massachusetts: Sinauer Associates. Version 4b10.
Tarrio R., Rodriguez-Trelles F., Ayala F. J. Shared nucleotide composition biases among species and their impact on phylogenetic reconstructions of the Drosophilidae. Mol. Biol. Evol. (2001) 18:459–468.
Teske P. R., Cherry M. I., Matthee C. A. The evolutionary history of seahorses (Syngnathidae: Hippocampus): molecular data suggest a West Pacific origin and two invasions of the Atlantic Ocean. Mol. Phylogenet. Evol. (2004) 30:459–468.
Thiel M. The zoogeography of algae-associated peracarids along the Pacific coast of Chile. J. Biogeogr. (2002) 29:999–1008.[CrossRef]
Vences M., Vieites D. R., Glaw F., Brinkmann H., Kosuch J., Veith M., Meyer A. Multiple overseas dispersal in amphibians. Proc. Roy. Soc. Lond. B (2003) 270:459–468.
Wang X., He S., Chen Y. Sequence variations of the S7 ribosomal protein gene in primitive cyprinid fishes: implication on phylogenetic analysis. Chinese Sci. Bull. (2002) 47:459–468.
Waters J. M., Dijkstra L. H., Wallis G. P. Biogeography of a Southern Hemisphere freshwater fish: how important is marine dispersal? Mol. Ecol. (2000a) 9:1815–1821.[Medline]
Waters J. M., López J. A., Wallis G. P. Molecular phylogenetics and biogeography of galaxiid fishes (Osteichthyes: Galaxiidae): dispersal, vicariance, and the position of Lepidogalaxias salamandroides. Syst. Biol. (2000b) 49:777–795.
Waters J. M., Wallis G. P. Cladogenesis and loss of the marine life-history phase in freshwater galaxiid fishes (Osmeriformes: Galaxiidae). Evolution (2001) 55:459–468.[CrossRef][Web of Science][Medline]
Webber W. R., Booth J. D. A new species of Jasus (Crustacea: Decapoda: Palinuridae) from the eastern South Pacific Ocean. N. Z. J. Mar. Freshw. Res. (1995) 29:459–468.
Wheeler W. C., Cartwright P., Hayashi C. Y. Arthropod phylogeny: a combined approach. Cladistics (1993) 9:459–468.
Whittaker R. J. Island biogeography: ecology, evolution, and conservation (1998) New York: Oxford University Press.
Williams S. T., Reid D. G., Littlewood D. T. J. A molecular phylogeny of the Littorininae (Gastropoda: Littorinidae): unequal evolutionary rates, morphological parallelism, and biogeography of the Southern Ocean. Mol. Phylogenet. Evol. (2003) 28:459–468.
Yoder A. D., Irwin J. A., Payseur B. A. Failure of the ILD to determine data combinability for slow loris phylogeny. Syst. Biol. (2001) 50:459–468.
Zardoya R., Doadrio I. Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. J. Mol. Evol. (1999) 49:459–468.
Zhang D. X., Hewitt G. M. Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol. Evol. (1996) 11:459–468.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||