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JOURNAL OF , 23(1): 169–177, 2003

MOLECULAR AND OF SOME OF AUSTRALIAN PALAEMONID

Nicholas P. Murphy and Christopher M. Austin

School of and Environment, Deakin University, P.O. Box 423, Warrnambool 3280, Australia (e-mail: [email protected])

ABSTRACT The evolutionary history and classification of the palaemonid shrimps has been the subject of constant speculation and debate. At present, all systematic treatments have been based on morphological characteristics. To help resolve the phylogenetic relationships, and thus enable the creation of a classification system that reflects evolutionary history, a region of the 16S mitochondrial rRNA gene was sequenced for a number of Australian . The resulting phylogenetic analyses indicated the presence of major anomalies in the current classification of Australian Palaemonidae. Significantly, three species belonging to three separate genera, intermedium, serenus, and australis, are closely related, with genetic differences more characteristic with that of congeneric species. The results also demonstrate non- in Australian palaemonids with respect to both Palaemonetes and Macrobrachium.

The Palaemonidae of shrimps is a the Palaemonidae, both within and between very successful group of decapods, inhabiting genera. The only phylogenetic study to focus on marine, estuarine, and freshwater environments the palaemonids as a whole was by Pereira throughout the world. The Palaemonidae are (1997), who performed a cladistic analysis of currently divided into four , the morphological characteristics. The majority of Palaemoninae, Pontoniinae, Euryrhynchinae, other studies have focused on the Macro- and Typhlocaridinae, with the first containing brachium, the largest within the perhaps the most familiar palaemonid genera: Palaemoninae (containing approximately 65% Macrobrachium, Palaemon, and Palaemonetes. of the species within subfamily) (Hedge- Whilst it is generally considered that the fam- cock et al., 1979; Lindenfelser, 1984; Mashiko ily Palaemonidae represents a natural group and Namuchi, 1993; Short, 2000; Murphy and (Pereira, 1997), the relationships within the fam- Austin, unpublished). Of these, Short (2000) pre- ily are far from clear. sents the most comprehensive phylogenetic study There have been many acknowledged prob- using morphological, biological, and ecological lems associated with the classification of the characters to assess the evolutionary relation- Palaemonidae. These occur at the specific ships of 30 Australian and non-Australian species (Lindenfelser, 1984; Short, 2000), generic (Hol- of Macrobrachium and nine species of related thuis, 1952; Fincham, 1987; Short, 2000), and genera of the Palaemoninae. Both Short (2000) family (Boulton and Knott, 1984; Pereira, 1997) and Pereira (1997) found evidence for anomalies levels. The problems have been attributed to dif- within the current taxonomic classification of ficulties in the interpretation of the significance the palaemonids. Pereira (1997) concluded that of morphological characteristics used to classify although the family Palaemonidae represents palaemonid and have hindered the de- a monophyletic group, several major lineages velopment of stable classification systems. within this family are, in fact paraphyletic. Short Holthuis(1950,1952)establishedthemostwidely (2000) provided further evidence that the current used classification of the Palaemonidae based on classification does not accurately reflect evolu- a number of morphological characteristics. How- tionary history, by identifying polyphyletic ever, this scheme has been criticized for not relationships within the genus Macrobrachium. accurately reflecting evolutionary relationships Until recently, all major systematic treat- within the group (Chace, 1972; Pereira, 1997). ments of palaemonids have been based on Recently, attempts have been made to de- morphological characteristics alone (Holthuis, velop hypotheses for the evolutionary history of 1950; Riek, 1951; Holthuis, 1952; Bray, 1976;

169 170 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 1, 2003

Choy, 1984; Fincham, 1987; Chace and Bruce, long debated, with a particular focus upon the 1993; Pereira, 1997), with the exception of representatives of the genus Palaemonetes Short (2000), who included some biological and in southwest Australia. Palaemonetes is repre- ecological characters. A few allozyme-based sented by two species in Australia, the largely studies have been undertaken (Trudaeu, 1978; estuarine Palaemonetes atrinubes and the Boulton and Knott, 1984; Lindenfelser, 1984; freshwater species Palaemonetes australis. Chow and Fujio, 1985a, b), but no phylogenetic (Bishop, 1967) suggested that Palaemonetes studies utilizing DNA-based have been originated in Australia from larvae carried published. This is surprising, given the world- across the Indian Ocean from Africa. It has wide distribution of the family and the fact that been said that the palaemonids, in general, several species, including the giant freshwater appear to be in transition from marine to prawn Macrobrachium rosenbergii, are impor- freshwater environments (Hedgepeth, 1957). tant commercially, particularly in developing However Boulton and Knott (1984) suggest, countries. In contrast, other important decapod based on allozyme data, that the likely ancestor crustacean groups, such as penaeid prawns, of Palaemonetes australis is a M. intermedium- freshwater crayfish, and marine , have like . been much more extensively studied using To further explore the taxonomic, phyloge- molecular genetic techniques (Palumbi and netic, and biogeographic questions pertaining to Benzie, 1991; Bouchon et al., 1994; Harding Australian palaemonids, sequencing of the 16S et al., 1997; Ovendon et al., 1997; Grandjean mtDNA gene region was undertaken. The 16S et al., 1998; Sarver et al., 1998; Crandall et al., mtDNA gene region has been found to be 1999). The use of DNA sequence data has the extremely useful for studying taxonomic ques- great advantage that it allows the creation of tions and phylogenetic relationships within a phylogeny that enables the testing of mor- a number of decapod crustacean groups phologically based systematic hypotheses and (Bucklin et al., 1995; Crandall and Fitzpatrick, for the independent assessment of morpholog- 1996; Ovendon et al., 1997; Kitaura et al., ical . 1998; Tam and Kornfield, 1998; Crandall et al., In Australia, palaemonids are widespread, 1999). The 16S rRNA gene has both fast- and with representatives inhabiting marine, estua- slow-evolving regions and therefore can provide rine, and freshwater environments. In prelimi- useful information across a broad taxonomic nary work on the phylogenetics of Australian spectrum from the population to the family Macrobrachium sp. using 16S mitochondrial level. DNA (mtDNA) sequences, Murphy and Austin The object of this paper is to essentially (2002) showed evidence for the non-monophyly follow up Boulton and Knott’s (1984) allo- within Australian Macrobrachium. Murphy and zyme study of Palaemonidae in the River Austin (2002) found that Macrobrachium Estuary, Western Australia, using powerful intermedium did not share a close evolution- DNA-based analyses. In addition to the samples ary relationship with other Australian Macro- examined by Boulton and Knott, specimens of brachium and instead was found to share Palaemon serenus and M. intermedium from a closer affinity with Palaemon serenus. eastern Australia and M. australiense and Boulton and Knott (1984), in a study of M. rosenbergii are included for comparative palaemonid species in the Swan River Estuary, purposes. Western Australia, also found inconsistencies between the current morphologically based MATERIALS AND METHODS classification system and genetic relation- ships between the species studied using allo- Taxa zyme data. Boulton and Knott (1984) showed The four Australian palaemonid species studied by M. intermedium to be closely allied to an- Boulton and Knott (1984), Macrobrachium intermedium (Stimpson, 1860); Palaemon serenus (Milne-Edwards, other species, Palaemonetes australis, suggest- 1837); Palaemonetes australis (Bray, 1976); and Palae- ing that they may be congeners. Short (2000) monetes atrinubes (Dakin, 1915) from the Swan River and Pereira (1997) also found evidence that estuary, Western Australia, were included in this study. M. intermedium is polyphyletic with respect to Also included were M. intermedium and P. serenus from . Warrnambool, , to allow for intraspecific compar- Macrobrachium isons, and M. australiense (Ortman, 1891) from inland The biogeographic relationships and the Australia and M. rosenbergii (De Man, 1879) from Papua origin of Australian palaemonids have been New Guinea to allow for species-level comparisons with MURPHY AND AUSTIN: MOLECULAR PHYLOGENY OF AUSTRALIAN PALAEMONIDAE 171

Macrobrachium. Macrobrachium intermedium is found were purified using a QIAGEN QIAquick PCR Purification in estuarine and some marine waters around the south- Kit, with final elution volumes of 50 ll per individual. The ern Australian coastline from Perth, W.A., to the central DNA concentrations were approximated against a Promega Queensland coast; P. serenus, a marine species, has a similar DNA/Hae 111 marker on a 2% agarose/TAE gel containing distribution. The two Palaemonetes species are found only ethidium bromide and viewed under UV light. in Western Australia; Palaemonetes australis is generally Samples were sent to the Australian Genome Research found in freshwater and upper estuaries in south-west Facility (AGRF), University of Queensland, for sequencing. Western Australia, whilst Palaemonetes atrinubes inhabits Sequencing reactions followed the protocol of Perkin Elmer, coastal embayments and lower estuarine environments along using an ABI big dye terminator reaction with custom eastern and western Australian coastlines and has also been primers. For each sample, sequencing was performed in both recorded in New Caledonia. The atyid shrimp directions. australiensi, was included as the species. As the evolutionary affinities of the species studied are relatively Phylogenetic Reconstruction unknown, it was decided that the outgroup should initially Sequence chromatograms were viewed and edited be somewhat removed from the studied group. The atyids and the palaemonids are both members of the infraorder manually using a combination of EditView and MacClade . (Maddison and Maddison, 2000). Once edited, multiple An abbreviated description of the main morphological alignments were performed using Clustal X (Thompson features currently used to separate the three genera studied et al., 1997) with multiple alignment parameters of gap penalty equal to 10–15, and gap extension penalty equal to are as follows: 3–5. Alignments were then checked and verified manually 1. Hepatic spine absent, branchiostegal spine present using MacClade; positions of uncertain alignment were ...... 2 excluded to produce a stable data set (Gatesy et al., 1993) – Hepatic spine present, branchiostegal spine absent and ensure that orthologous characters were compared. Se- ...... Macrobrachium quences were then imported into PAUP 4.0b4a (Swofford, 2. No mandibular palp present ...... Palaemonetes 1998) for phylogenetic analysis. Three methods of – Mandibular palp present ...... Palaemon building were used: maximum-likelihood, maximum parsi- mony, and . Heuristic searches were employed for both maximum-likelihood and maximum Sample Collection parsimony using random sequence addition to eliminate any bias from sequence addition; confidence in all was Macrobrachium intermedium was collected from sea- calculated by nonparametric bootstrapping. grass beds in the estuarine sections of the Fitzroy River The appropriate model of evolution for maximum- in southwest Victoria and Swan River, Perth, Western likelihood (ML) analysis was obtained via testing alternative Australia. Palaemon serenus was obtained from rock pools modes of evolution using Modeltest (Posada and Crandall, off Griffith Island, Port Fairy, Victoria, and Mandurah, 1998). Modeltest obtains a starting tree via neighbor joining; Western Australia. Palaemonetes australis was obtained different models of evolution are then tested with this tree from the upper Swan River, whilst Palaemonetes atrinubes topology, and likelihood scores are calculated and compared was collected from the lower Swan River estuary. Macro- statistically. On the basis of these tests, the TrN 1 G model brachium australiense was collected from the Murray River, of sequence evolution was chosen, and the parameters N.S.W., and Macrobrachium rosenbergii was collected specified by this model were used to estimate a tree via the from a small river near Madang, Papua New Guinea. All maximum-likelihood method. Specifically the parameters specimens were collected using a dipnet and were either used were a rate matrix of (A-C) 5 1.0000, (A-G) 5 4.5195, frozen in liquid nitrogen immediately and stored in 95% (A-T) 5 1.0000, (C-G) 5 1.0000, (C-T) 5 9.6383, (G-T) 5 ethyl alcohol or transported live back to the laboratory and 1.0000; base frequencies of A 5 0.306, C 5 0.108, G 5 stored at 2808C. Voucher specimens were stored in 70% 0.216, T 5 0.371; gamma distribution parameter 5 0.1542. ethanol and are currently housed on site (Deakin University, Heuristic searches were used with 1,000 sequence additions, School of Ecology and Environment, Molecular Ecology whilst bootstrappings consisted of 100 replications with 100 Lab), until the completion of this study, whereupon they will sequence additions. Maximum-parsimony analyses were be housed in an appropriate Australian museum. performed with gaps treated as missing, heuristic searches as per maximum-likelihood analyses; however, 1,000 boot- DNA Extraction and Amplification strapreplicateswereperformedeachwith1,000se- quence additions. A neighbor-joining tree was constructed DNA was extracted from abdominal muscle tissue us- with distances calculated under the Tamura-Nei model of ing a high salt precipitation method (Crandall et al., 1999). nucleotide sequence evolution; bootstrapping was performed A fragment of the 16S rRNA mitochondrial gene was with 1,000 replicates. A distance matrix was also created amplified by PCR using universal 16S mtDNA primers using the above model. (16Sar and 16Sbr). Double-stranded PCR products were obtained in a total reaction volume of 50 ll, containing 5 ll Phylogenetic Hypothesis Testing of 10X PCR buffer, 0.4 mM of each dNTP, 0.8 lM of each primer, 4 mM MgCl2, 1 unit of Taq polymerase and 2 ll To test phylogenetic hypotheses, comparisons were made of DNA extract. The PCR amplification was carried out in between optimal trees and trees developed using topological a Corbett Palm-Cycler using the following temperature constraints. The non-parametric test of Templeton (1983) regime: an initial denaturation step of 958C for 3 min, was used to compare maximum parsimony trees. Maximum- followed by 30 cycles of 958C for 30 seconds (s), an parsimony estimates were carried out in PAUP* for annealing temperature of 508C for 30s, and an extension alternative phylogenetic hypotheses by enforcing topologi- temperature of 728C for 30s. This was then followed by an cal constraints developed in MacClade. A one-tailed additional extension of 728C for 3 min. The PCR products Templeton (1983) test was carried out in PAUP* to 172 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 1, 2003

Fig. 1. Consensus phylogram* from maximum-parsimony, neighbor-joining, and maximum-likelihood analyses. Bootstrap values for each analysis are shown in the above (2 means , 50% bootstrap support) (* actual topology shown is that of neighbor joining analysis). determine significant differences in tree length. An analysis RESULTS of maximum-likelihood hypotheses was carried out via parametric bootstrapping and subsequent comparisons of The sequence alignment, after the removal of likelihood ratios (Hillis et al., 1996; Huelsenbeck and regions of ambiguous alignment, yielded a total Crandall, 1997; Goldman et al., 2000). A parametric of 494 sites for phylogenetic analysis, of which bootstrap was implemented by comparing the likelihood 206 were variable. The mean total nucleotide ratio between the optimal tree created by PAUP* and the composition was A 5 30%, T 5 35%, C 5 13% null hypothesis tree with likelihood ratios of optimal and null hypothesis trees from simulated data sets created and G 5 22%, indicating that the 16s RNA essentially via Monte Carlo simulation of DNA sequence region of the mtDNA is adenosine- and evolution (Rambaut and Grassly, 1997). One hundred thymine-rich in the palaemonids. No significant replicate data sets with the same tree topology and branch differences in base composition across all taxa lengths as the null hypothesis tree were generated using the 2 same parameters and model of sequence evolution as were detected (v 5 9.517, d.f. 5 27, P 5 estimated for the observed data (Jarman et al., 2000b) and 0.99). Resulting sequences have been submitted with the same number of sites. to Genbank (AF439515–AF439523).

Table 1. The Tamura-Nei pairwise distances (below) and number of nucleotide substitutions (above) among the specimens studied.

1. 2. 3. 4. 5. 6. 7. 8. 9. 1. M. intermedium (Vic) — 8 29 41 42 59 108 105 160 2. M. intermedium (WA) 0.017 — 30 43 43 60 107 105 159 3. Palaemonetes australis 0.063 0.065 — 39 38 61 108 104 160 4. P. serenus (Vic) 0.091 0.096 0.087 — 5 53 107 111 162 5. P. serenus (WA) 0.093 0.096 0.084 0.010 — 50 105 110 158 6. Palaemonetes atrinubes 0.135 0.137 0.140 0.145 0.137 — 116 109 156 7. M. australiense 0.269 0.266 0.269 0.266 0.263 0.293 — 43 138 8. M. rosenbergii 0.261 0.261 0.257 0.278 0.275 0.273 0.097 — 145 9. 0.445 0.441 0.445 0.456 0.439 0.429 0.370 0.392 — MURPHY AND AUSTIN: MOLECULAR PHYLOGENY OF AUSTRALIAN PALAEMONIDAE 173

Phylogenetic Analyses The construction of phylogenetic trees re- sulted in three equivalent topologies (Fig. 1). Bootstrap confidence levels were generally high for all nodes within the tree; the neighbor joining and maximum parsimony trees showing strong support for two . One contains Macrobrachium intermedium, Palaemonetes australis, and Palaemon serenus, with Palae- monetes atrinubes in the most position. A second containing M. australiense and M. rosenbergii was also strongly supported; there was no support for a relationship between these two species and M. intermedium apparent. The maximum-likelihood analysis identified the same major clades but with generally lower levels of bootstrap support, especially in re- lation to the position of P. serenus (, 50% support). The Tamura-Nei pairwise distance matrix and absolute base difference (Table 1) shows the degree of divergence between M. intermedium, Palaemonetes australis, and P. serenus to be very similar (0.063–0.093), whilst Palaemo- netes atrinubes is equally distant from all of these species (; 0.150). The degree of di- vergence between the two other Macro- brachium species, M. australiense and M. rosenbergii (0.097), is comparable with the genetic divergence between M. intermedium, Palaemonetes australis, and P. serenus, whilst the distance between these two clades is much larger (0.258–0.293).

Tests of Phylogenetic Hypotheses Using the maximum-parsimony and maxi- mum-likelihood procedures, the 16S mtDNA sequence data were used to test four phyloge- netic hypotheses in relation to the species studied. The hypotheses tested were: a) that the three Macrobrachium species are mono- phyletic; b) that the two Palaemonetes species Fig. 2. Some phylogenetic hypotheses based on the studied are monophyletic; c) the phylogenetic species studied. Short (2000) and Pereira (1997) indicate relationships suggested by Short (2000) (a representative topologies based on their more extensive Palaemon/Palaemonetes clade and Macro- studies. brachium polyphyletic with respect to M. inter- medium); and d) the relationships suggested by Pereira (1997) (M. intermedium the most basal ratios (d) (Huelsenbeck and Crandall, 1997; group). These hypotheses are represented as Goldman et al., 2000) (Fig. 3) also led to all in Fig. 2. hypotheses being rejected (P , 0.001). Thus, From Table 2, it can be seen that these all phylogenetic hypotheses tested resulted in hypotheses are all rejected (P , 0.001) using trees with topologies highly inconsistent (either Templeton’s test and maximum parsimony. longer tree length or smaller Ln-likelihood) with Parametric bootstrapping of the log-likelihood the optimal trees. 174 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 1, 2003

Table 2. Templeton (1983) tests for significant differences in maximum parsimony tree lengths for the optimal tree versus constraint trees.

Constraint Length Rank sums nZ P Optimal 355 Macrobrachium 389 877.5 44 25.1257 ,0.0001* 2112.5 Palaemonetes 365 157.5 20 22.2361 0.0253* 252.5 Short (2000) 365 133.0 18 22.3570 0.0184* 238.0 Pereira (1997) 393 927.5 45 25.1632 ,0.0001* 2107.5

* Significance at a 5 0.05.

DISCUSSION group are uncertain. It may be a distinct The results of this study indicate that the Australian of coastal palaemonids or current classification of Australian Palaemoni- part of a more widespread lineage. The position nae is questionable and that both Macrobra- of Palaemonetes atrinubes within the Palae- chium and Palaemonetes are not monophyletic. monidae is also unclear. Bray (1976) claimed It also appears that Macrobrachium inter- that Palaemonetes atrinubes, with the excep- medium, Palaemonetes australis,andPalaemon tion of one character linking this species with serenus form a natural group. Genetic diver- Palaemonetes australis, did not appear closely gences among these species, when compared related to other Australian species. The results with the genetic divergences between M. of this study are consistent with this observation australiense and M. rosenbergii and those of indicating it is phylogenetically distinct from other studies of the 16S mtDNA region in the three other ‘‘coastal palaemonid’’ species In- Crustacea (Suno-Ughi et al., 1997; Ponniah and creased sampling of palaemonid shrimps Hughes, 1998; Jarman et al., 2000a; Tong et al., within and outside Australia is currently being 2000), are typical of those found between con- undertaken to clarify phylogenetic questions generic species. This reinforces Boulton and pertaining to palaemonid species worldwide. A Knott’s (1984) view that Palaemonetes aus- better representation of species, including tralis is congeneric with M. intermedium, based species of these genera, will allow for a better on allozyme electrophoresis. Therefore, mor- understanding and may well change the rela- phological features currently used to separate tionships between the taxa studied. these three genera (i.e., hepatic/branchiostegal These findings have implications for pre- spine and mandibular palp) are phylogenetically vious evolutionary analyses of morphological, unreliable and plastic. history, and physiological traits in these These results are not altogether surprising shrimps. For example, many comparisons of and are consistent with other studies suggest- larval life cycles across Macrobrachium shrimp ing problems with the current classification of have been made, many of which have included Australian palaemonids. (Boulton and Knott, M. intermedium (Holthuis, 1952; Williamson, 1984; Fincham, 1987; Short, 2000). On the 1972; Greenwood et al., 1976). Our results basis of allozyme electrophoresis, Boulton and indicate it would be more appropriate to Knott (1984) found Palaemonetes australis to compare M. intermedium larval life stages and be closely related to Macrobrachium interme- life history with those of Palaemon serenus and dium, but the wider relationships of these Palaemonetes australis. Similarly, in relation to species could not be determined, as no other , it appears that undue emphasis has species of Macrobrachium, for example, were been placed on the taxonomic significance of included in their data set. Other studies have the presence and absence of the hepatic and found Macrobrachium to be polyphyletic with branchiostegal spines in defining the genera respect to M. intermedium (Pereira, 1997; Short, Macrobrachium, Palaemo, and Palaemonetes. 2000; Murphy and Austin, 2002). Phylogenetic analyses are also necessary for The wider evolutionary affinities of the P. a proper understanding of the biogeographic serenus/Palaemonetes australis/M. intermedium history of . The presence of the MURPHY AND AUSTIN: MOLECULAR PHYLOGENY OF AUSTRALIAN PALAEMONIDAE 175

the coastal fringe of southeastern Australia. This is most likely due to the presence of the atyid shrimp Paratya australiensis in eastern coastal freshwater systems, which appears to exploit a similar freshwater niche. The origin of Australian Macrobrachium is a similarly de- bated topic. Bishop (1967) suggested that they most likely originated from Asia and then dispersed throughout eastern Australia, whilst Williams (1981) proposed that some Australian species may have evolved relatively recently from in situ marine ancestors. It is certain from the results of this study that if Williams’ (1981) theory is correct, then the marine ancestral form of Australian Macrobrachium is not M. inter- medium. This study provides clear evidence that current generic classification of Australian Palaemoninae is invalid. As a consequence, it raises some intriguing questions regarding the taxonomic validity of these genera more widely and the evolutionary affinities and biogeo- graphic relationships of Australian palaemonid shrimps. Thus, there is much scope for further study of the of palae- monid shrimps. This should not be restricted purely to Australian species, but needs to encompass species worldwide. Such studies would allow for greater understanding of the taxonomic and phylogenetic relationships of these species and generate new perspectives on the evolutionary, morphological, and life history variation in these shrimps.

ACKNOWLEDGEMENTS N. P. Murphy was supported by an Australian Post- graduate Award. We thank Thuy Nguyen, Lachlan Farring- ton, Adam , Paul Jones, and Bob Collins for assistance in collecting samples. Fig. 3. Likelihood-ratio (d) tests for monophyly. The observed value of d for trees constrained to equal LITERATURE CITED phylogenetic hypotheses and optimal trees compared to Bishop, J. A. 1967. The zoogeography of the Australian the distribution of d generated via 100 Monte Carlo freshwater decapod Crustacea. Pp. 107–122 in A. H. simulations. Weatherly, ed. Australian Inland Waters and Their Fauna. Australian National University Press: Canberra. Bouchon, D., C. Souty-Grosset, and R. Raimond. 1994. Palaemonetes australis in southwest Western Mitochondrial DNA variation and markers of species Australian rivers has long been recognized as identity in two penaeid shrimp species.—Aquaculture a biogeographic conundrum. The results of this 127: 131–144. Boulton, A. J., and B. Knott. 1984. Morphological and study support Boulton and Knott’s (1984) electrophoretic studies of the Palaemonidae (Crustacea) of theory of the invasion of unexploited freshwater the Perth region, Western Australia.—Australian Journal by a nearshore marine ancestor, pro- of Marine and Freshwater Research 35: 769–783. bably of a M. intermedium-like form. While Bray, D. M. 1976. A review of two Western Australian shrimps of the genus Palaemonetes, P. australis Dakin M. intermedium occurs along the entire southern 1915 and P. atrinubes Sp. Nov. (, Palae- Australian coastline, there is no closely related monidae).—Records of the Western Australian Museum palaemonid species in freshwater systems along 4: 65–84. 176 JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 23, NO. 1, 2003

Bucklin, A., B. W. Frost, and T. D. Kocher. 1995. . 2nd ed. Sinauer Associates, Sunderland, Molecular systematics of six Calanus and three Metridia Massachusetts. species.— 121: 655–664. Holthuis, L. B. 1950. The Palaemonidae collected by the Chace, F. A., Jr. 1972. from Hawaii and Siboga and Snellius Expeditions, with remarks on other the status of the genus Palaemonetes (Decapoda, Palae- species. The Decapoda of the Siboga Expedition. Part X. monidae).—Crustaceana 23: 13–19. The Palaemonidae. I Subfamily Palaemoninae.—Siboga- ———, and A. J. Bruce. 1993. The caridean shrimps Expeditie, Leiden 39(a): 1–268. (Crustacea: Decapoda) of the Philippine ———. 1952. A general revision of the Palaemonidae expedition, 1907–1910, Part 6: Superfamily Palaemonio- (Crustacea, Decapoda, Natantia) of the Americas. II. The dea.—Smithsonian Contributions to 292: 1–152. subfamily Palaemoninae.—Occasional Papers of the Chow, S., and Y. Fujio. 1985a. Population of the Allan Hancock Foundation 12: 1–396. Palaemonid shrimps (Decapoda: Crustacea) I. Genetic Huelsenbeck, J. P., and K. A. Crandall. 1997. Phylogeny variability and differentiation of local populations.— estimation and hypothesis testing using maximum likeli- Tohoku Journal of Agricultural Research 36: 93–108. hood.—Annual Review of Ecology and Systematics 28: ———, and ———. 1985b. of the 437–466. palaemonid shrimps (Decapoda: Crustacea) II. Genetic Jarman, S. N., N. G. Elliot, S. Nicol, and A. McMinn. variability and differentiation of species.—Tohoku Jour- 2000a. Molecular phylogenetic studies of circumglobal nal of Agricultural Research 36: 109–116. species (Euphausiacea: Crustacea).—Canadi- Choy, S. C. 1984. On the freshwater palaemonid prawns an Journal of Fisheries and Aquatic 57: 51–58. from the Fiji islands (Decapoda, Caridea).—Crustaceana ———, S. Nicol, N. G. Elliott, and A. McMinn. 2000b. 28S 47: 269–277. rDNA evolution on the Eumalacostraca and the phyloge- Crandall, K. A., J. W. Fetzner, S. H. Lawler, M. Kinnersley. netic position of .—Molecular Phylogenetics and and C. M. Austin. 1999. Phylogenetic relationships Evolution 17: 26–36. among the Australian and New Zealand genera of Kitaura, J., K. Wada, and M. Nishida. 1998. Molecular freshwater crayfishes.—Australian Journal of Zoology phylogeny and evolution of unique mud-using territorial 47: 199–214. behavior in ocypodid (Crustacea: Brachyura: ———, and J. F. Fitzpatrick. 1996. Crayfish molecular Ocypodidae).— and Evolution 15: systematics: using a combination of procedures to 626–637. estimate phylogeny.—Systematic Biology 45: 1–26. Lindenfelser, M. E. 1984. Morphometric and allozyme Fincham, A. A. 1987. A new species of Macrobrachium congruence: evolution in the prawn Macrobrachium (Decapoda, Caridea, Palaemonidae) from the Northern rosenbergi (Decapoda: Palaemonidae).—Systematic Zoology 33: 195–204. Territory, Australia and a key to Australian species of the Maddison, D. R., and W. P. Maddison. 2000. MacClade 4: genus.—Zoologica Scripta 16: 351–354. Analysis of Phylogeny and Character Evolution. Version Gatesy, J., R. Desalle, and W. Wheeler. 1993. Alignment- 4.0. Sinauer Associates, Sunderland, Massachusetts. ambiguous nucleotide sites and exclusion of systematic Mashiko, K., and K. Namuchi. 1993. Genetic evidence for data.—Molecular Phylogenetics and Ecology 2: 152–157. the presence of a distinct freshwater prawn (Macro- Goldman, N., J. P. Anderson, and A. G. Rodrigo. 2000. brachium nipponense) populations in a single river Likelihood-based tests of topologies in phylogenetics.— system.—Zoological Science 10: 161–167. Systematic Biology 49: 652–670. Murphy, N. P., and C. M. Austin. 2002. A preliminary study Grandjean, F., N. Gouin, M. Frelon, and C. Souty-Grosset. of 16S rRNA sequence variation in Australian Macro- 1998. Genetic and morphological systematic studies on brachium shrimps (Palaemonidae: Decapoda) reveals the crayfish pallipes.—Journal of inconsistencies in their current classification.—Inverte- Crustacean Biology 18: 549–555. brate Systematics 16: 697–701. Greenwood, J. G., D. L. Fielder, and M. J. Thorne. 1976. Ovendon, J. R., J. D. Booth, and A. J. Smolenski. 1997. The larval life history of Macrobrachium novaehollan- Mitochondrial DNA phylogeny of red and green rock diae (De Mann) (Decapoda, Palaemonidae), reared in the lobsters.—Marine and Freshwater Research 48: 1131– laboratory.—Crustaceana 30: 252–286. 1136. Harding, G. C., E. L. Kenchington, C. J. , C. S. Palumbi, S. R., and J. Benzie. 1991. Large mitochondrial Pezzack, and D. C. Landry. 1997. Genetic relationships DNA differences between morphologically similar pe- among subpopulations of the American ( naeid shrimp.—Molecular Marine Biology and Biotech- americanus) as revealed by random amplified poly- nology 1: 27–34. morphic DNA.—Canadian Journal of Fisheries and Pereira, G. 1997. A cladistic analysis of the freshwater Aquatic Science 54: 1762–1771. shrimps of the family Palaemonidae (Crustacea, Deca- Hedgecock, D., D. J. Stelmach, K. Nelson, M. E. poda, Caridea).—Acta Biologica Venezuelica 17: 1–69. Lindenfelser, and S. R. Malecha. 1979. Genetic di- Ponniah, M., and J. M. Hughes. 1998. Evolution of vergence and of natural populations of Queensland spiny mountain crayfish of the genus Macrobrachium rosenbergi.—Proceedings of the World Clark (Decapoda: ): preliminary Mariculture Society 10: 873–879. 16S mtDNA phylogeny.—Proceedings of the Linnean Hedgpeth, J. W. 1957. Biological Aspects. Pp. 673–749 in Society of New South Wales 119: 9–19. J. W. Hedgpeth, ed. Treatise on Marine Ecology and Posada, D., and K. A. Crandall. 1998. MODELTEST: . Memoirs of the American Geological testing the model of DNA substitution.— Society 67. 14: 817–818. Hillis, D. M., B. K. Mable, and C. Moritz. 1996. Rambaut, A., and N. C. Grassly. 1997. Seq-Gen: an Applications of molecular systematics: the state of the application for the Monte Carlo simulation of DNA field and a look at the future. Pp. 515–543 in sequence evolution along phylogenetic trees.—Computer D. M. Hillis, C. Moritz, and B. K. Mable, eds. Molecular Applications in the Biosciences 13: 235–238. MURPHY AND AUSTIN: MOLECULAR PHYLOGENY OF AUSTRALIAN PALAEMONIDAE 177

Riek, E. F. 1951. The Australian freshwater prawns of the Analysis of DNA Sequence Data. Marcel Dekker, New family Palaemonidae.—Records of the Australian Muse- York. um 22: 358–367. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, Sarver, S. K., J. D. Silberman, and P. J. Walsh. 1998. and D. G. Higgens. 1997. The ClustalX windows Mitochondrial DNA sequence evidence supporting the interface: flexible strategies for multiple sequence align- recognition of two or species of the Florida ment aided by quality analysis tools.—Nucleic Acids .—Journal of Crustacean Biology 18: Research 24: 4876–4882. 177–186. Tong, J. G., T. Y. Chan, and K. H. Chu. 2000. A prelimin- Short, J. 2000. Systematics and biogeography of Australian ary phylogenetic analysis of Metapenaeopsis (Decapoda: Macrobrachium (Crustacea: Decapoda: Palaemonidae)– Penaeidae) based on mitochondrial DNA sequences of with descriptions of other new freshwater Decapoda. selected species from the Indo-West Pacific.—Journal of Ph.D. Thesis, The University of Queensland. Brisbane. Crustacean Biology 20: 541–549. Suno-Ughi, N., F. Sasaki, S. Chiba, and M. Kawata. 1997. Trudaeu, T. N. 1978. Electrophoretic protein variation in and its implications in genetic Morphological stasis and phylogenetic relationships in studies.—Proceedings of the World Mariculture Society tadpole shrimps, (Crustacea: ).— 9: 139–145. Biological Journal of the Linnean Society 61: 439–457. Williams, W. D. 1981. The Crustacea of Australian inland Swofford, D. L. 1998. PAUP*. Phylogenetic Analysis Using waters. Pp 1108–1138 in A. Keast, ed. Biogeography of Parsimony (*and Other Methods). Version 4. Sinauer, Australia. Dr W. Junk, The Hague. Sunderland, Massachusetts. Williamson, D. I. 1972. Larval development in a marine and Tam, Y. K., and I. Kornfield. 1998. Phylogenetic relation- freshwater species of Macrobrachium (Decapoda, Palae- ships of clawed lobster genera (Decapoda: Nephropidae) monidae).—Crustaceana 23: 282–298. based on mitochondrial 16s rRNA gene sequences.— Journal of Crustacean Biology 18: 138–146. Templeton, A. R. 1983. and non- parametric inferences from restriction fragment and DNA RECEIVED: 13 November 2001. sequence data. Pp. 151–179 in B. Weir, ed. Statistical ACCEPTED: 1 May 2002.