African Journal of Marine Science 2007, 29(2): 253–258 Printed in South Africa — All rights reserved

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AFRICAN JOURNAL OF MARINE SCIENCE EISSN 1814–2338 doi: 10.2989/AJMS.2007.29.2.9.192

Phylogeographic structure of the caridean shrimp Palaemon peringueyi in South Africa: further evidence for intraspecific genetic units associated with marine biogeographic provinces PR Teske1*, PW Froneman2, NP Barker1 and CD McQuaid2 1

Molecular Ecology and Systematics Group, Department of Botany, Rhodes University, Grahamstown 6140, South Africa Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa * Corresponding author, e-mail: [email protected]

2

Recent genetic studies have shown that most widely distributed, passively dispersing invertebrates in southern Africa have regional intraspecific units that are associated with the three main marine biogeographic provinces (cool-temperate, warm-temperate and subtropical). The caridean shrimp Palaemon peringueyi also occurs in all three provinces, but the fact that it can disperse both actively and passively (i.e. larval drifting, adult walking/swimming and potential adult rafting by means of floating objects) suggests that the amount of gene flow between regions may be

too high for evolutionary divergence to have taken place. Samples of P. peringueyi were collected throughout South Africa and an intraspecific phylogeny was reconstructed using mitochondrial COI and 16S rRNA sequences. Three major clades were recovered, which were broadly associated with the three biogeographic regions. This suggests that, even though P. peringueyi can disperse actively, the fact that neither larvae nor adults are strong swimmers has resulted in genetic subdivisons comparable to those of passively dispersing coastal invertebrates in southern Africa.

Keywords: genetic drift, larval retention, mitochondrial DNA COI and 16S rRNA, planktonic dispersal, population size fluctuation, rafting, swimming

Introduction The South African coast can be divided into three main marine biogeographic provinces that differ in terms of mean sea surface temperatures: the cool-temperate West Coast, warm-temperate South Coast, and subtropical East Coast (Stephenson and Stephenson 1972). The exact locations of the boundaries between these provinces are disputed. They vary for different taxa, and various regions of overlap and smaller-scale groupings have been proposed (reviewed in Harrison 2002). Moreover, there is evidence for a fourth (tropical) province in the extreme north-east of the country (Jackson 1976, Bolton et al. 2004, Teske et al. in press a). Although differences in species composition between the provinces have long been recognised, it has only recently been discovered that a number of coastal species that occur in more than one biogeographic province are characterised by genetic discontinuities that often coincide with the boundaries between the provinces. Species that have phylogeographic breaks between the cool-temperate and warmtemperate provinces include the mollusc Haliotis midae (Evans et al. 2004) and the crustaceans Upogebia africana and Exosphaeroma hylecoetes (Teske et al. 2006). Phylogeographic discontinuities between the warm-temperate and subtropical provinces have been found in the crustaceans U. africana and Hymenosoma orbiculare (Edkins et al. 2007, Teske et al. in press b), as well as in the molluscs

Patella granularis (Ridgway et al. 1998) and Perna perna (Zardi et al. 2007). Forces driving divergence of regional populations of coastal species may include currents, diversifying selection due to adaptation of regional populations to environmental conditions characteristic of a particular biogeographic province (e.g. temperature), low levels of gene flow owing to isolation by distance, competitive exclusion of sister lineages, or a combination of several of these (Teske et al. 2006, Zardi et al. 2007, Teske et al. in press b). The fact that all of the above coastal invertebrates disperse passively by means of either planktonic larval dispersal or adult rafting suggests that these modes of dispersal are insufficient to prevent genetic divergence among regional populations, possibly because by far the most recruitment occurs in the vicinity of the parent habitat (McQuaid and Phillips 2000, Teske et al. in press b). Species that employ active adult dispersal, on the other hand, tend to exhibit shallow population structuring or panmixia. Examples include the teleosts Argyrosomus japonicus and Pomadasys commersonnii (Klopper 2005), Rhabdosargus holubi (Oosthuizen 2006), as well as Atherina breviceps and Gilchristella aestuaria (Norton 2005). The estuarine round herring Gilchristella aestuaria is particularly interesting, because it completes its life cycle within estuaries with only sporadic dispersal into the marine

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habitat. Consequently, it is characterised by more genetic structure than other southern African coastal teleosts, but even so, it shows phylogeographic patterns that do not conform to the marine biogeographic provinces. This suggests that actively dispersing species may cross the boundaries between the provinces too frequently to allow for genetic divergence to occur. In the present study, we focused on a species that can be considered to be intermediate between the actively dispersing teleosts and the passively dispersing invertebrates, namely the caridean shrimp Palaemon peringueyi (Stebbing 1915), a species previously referred to as P. pacificus (Stimpson 1860) (Macpherson 1990). This shrimp is present in all three main marine biogeographic provinces, although there is some disagreement concerning its exact distribution. Broekhuysen and Taylor (1959) and de Villiers et al. (1999) report that it occurs from Walvis Bay (Namibia) on the West Coast to Kosi Bay on the east coast of South Africa, whereas Day (1974) gives East London as its eastern distribution limit (Figure 1). There are no specimens of P. peringueyi from the East Coast in the collections of the Iziko Museum, Cape Town (GM Branch and CL Griffiths, Zoology Department, University of Cape Town, pers. comm.), and during several sampling expeditions, the current authors have never found it north of Port St Johns (northern South-East coast, Figure 1). P. peringueyi has a marine adult phase and a juvenile phase that can either be completed in estuaries or in intertidal rock pools (Emmerson 1986). Breeding and early larval development occur in marine coastal waters. The last zoeal stage and the postlarvae then migrate to sheltered nursery habitats (Emmerson 1986). Juveniles spend between 9 and 12 months in these habitats, whereupon they return to the nearshore habitat (Wooldridge 1999). In

BOTSWANA

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0

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Figure 1: Map of South Africa showing sampling localities, marine biogeographic provinces and geographic localities mentioned in the text

addition to larval drifting and active adult dispersal by means of swimming or walking, the species may also disperse by means of rafting. Several palaemonid shrimps have been reported to disperse by means of floating objects such as macroalgae (Kingsford and Choat 1985, Wehrtmann and Dittel 1990), and the fact that P. peringueyi is often associated with wood (PRT pers. obs.) or seagrass (Emmerson 1986) suggests that rafting provides a likely additional mode of long-distance dispersal in this species. Although larval development and population dynamics of young P. peringueyi within estuaries and tidal rock pools are well understood (e.g. Emmerson 1983, 1985, Bernard and Froneman 2005, Froneman 2006), little is known about whether adult dispersal in this species is comparable to that of the coastal teleosts studied to date in terms of maintaining genetic connectivity between populations present in different marine biogeographic provinces. Most genetic studies on penaeid shrimps (which are probably very similar to palaemonid shrimps in terms of their dispersal potential) have found little population structuring (e.g. Ball and Chapman 2003, Borrell et al. 2004, Valles-Jimenez et al. 2005), but there are exceptions (Brooker et al. 2000, Weetman et al. 2007). To investigate this issue, we reconstructed phylogeographic patterns of P. peringueyi in South Africa using two mitochondrial DNA markers and compared them with those of actively and passively dispersing coastal animals. Material and Methods Between three and seven specimens of P. peringueyi per sampling locality were collected in all three main southern African marine biogeographic provinces (Figure 1). Phylogeographic patterns were identified by constructing intraspecific phylogenies using sequences of portions of the mitochondrial cytochrome oxidase c subunit 1 (COI) gene and the region coding for 16S rRNA. COI sequences were amplified with primers for decapod crustaceans (CrustCOIF 5’-TCA ACA AAT CAY AAA GAY ATT GG-3’ and DecapCOIR 5’-AAT TAA AAT RTA WAC TTC TGG-3’; Teske et al. 2006) and 16S rRNA sequences were obtained with universal primers 16SarL (5’-CGC CTG TTT ATC AAA AAC AT-3’) and 16SbrH (5’-CGG GTC TGA ACT CAG ATC ACG T-3’) (Palumbi 1996). Extraction, amplification and sequencing followed previously published protocols (Teske et al. 2004, 2006). Because phylogenetic trees reconstructed with COI and 16S rRNA sequences were congruent, phylogenetic analyses were conducted using combined sequence data from both markers. As an outgroup, we used sequences of palaemonid shrimps for which both COI and 16S rRNA sequences are available on GenBank (Palaemon longirostris: COI: AJ640124, 16S rRNA: AJ640129, A Cartaxena, Museu Nacional de História Natural, Lisbon, Portugal, unpublished data; Macrobrachium nipponense: COI: DQ656415, 16S rRNA: DQ656416, Salman et al. 2006). The COI sequences were trimmed to a length of 393 bp. Length differences in the 16S rRNA sequences were only found between M. nipponense and the remaining sequences (three indels, each one nucleotide in length). Following alignment using default parameters in CLUSTALX (Thompson et al. 1997), 16S rRNA sequences were trimmed to a length of 425 bp.

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The following three methods of phylogenetic reconstruction were used. First, a 50% majority rule consensus tree was constructed with MRBAYES version 3.1 (Huelsenbeck and Ronquist 2001). The Markov chain Monte Carlo process was set for four chains to run simultaneously for 5 000 000 generations, with trees being sampled every 100 generations. Suitable model priors for 16S rRNA were determined using AIC (Akaike 1973) in MRMODELTEST Version 2.2 (Nylander 2004). These were: Nst = 2, rates = invgamma, statefreqpr = dirichlet(1,1,1,1) (HKY+Γ+I model; Hasegawa et al. 1985). Each of the three character positions of COI was allowed to have its own rate by specifying the following settings: Nst = 6, rates = gamma, statefreqpr = fixed(equal), ratepr = variable. In addition to examining posterior probabilities of the resulting trees to determine by which generation burn-in was complete, we also compared standard errors of posterior probabilities between simultaneous runs. Because these tended to decrease for some time after the burn-in phase, only trees were used once the difference in standard errors had also stabilised (i.e. the first 25 000 trees were discarded). Bayesian analyses were repeated three times to ensure that results were consistent. Second, a neighbourjoining bootstrap tree was constructed in PAUP* version 4.0b10 (Swofford 2002) using a distance model determined for the combined COI and 16S rRNA sequences with M ODELTEST version 3.7 (Posada and Crandall 1998): TrN+Γ+I (α = 0.37, propinv = 0.63; Tamura and Nei 1993). Support for nodes was assessed based on 10 000 bootstrap replications and default settings were specified. Third, a parsimony bootstrap tree was reconstructed in PAUP* by specifying 10 random addition replications, 100 trees held at each step, and 10 000 bootstrap replications. Results In all, 12 COI haplotypes and seven 16S rRNA haplotypes were recovered from a sample of 42 specimens of P. peringueyi. These were submitted to GenBank (accession numbers EF595551–EF595569). The combined dataset comprised 13 haplotypes. Three major regional phylogeographic units of P. peringueyi were recovered (Figure 2). These were primarily defined by three well-supported clades (a West Coast clade present in the Olifants and Groot Berg estuaries and in Langebaan Lagoon, a South Coast clade present from the Gourits Estuary to the Mbhanyana Estuary, and a SouthEast Coast clade that was found in the region between the Mbhanyana and Mzimvubu estuaries). The three methods of phylogenetic reconstruction differed with regard to the clustering of the specimens from the Bot Estuary (SouthWest Coast), as well as the placement of three specimens from estuaries located in the warm-temperate biogeographic province. Bayesian inference grouped the samples from the Bot Estuary with the West Coast samples, a relationship that was strongly supported by a posterior probability of 96%. The placement of these samples was unresolved in the neighbour-joining and parsimony analyses (bootstrap values <50%). All three methods recovered a second South Coast clade (present in the Gourits and Keurbooms estuaries), the placement of which among other

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clades was unresolved, but whose distinctness from the well-supported South Coast clade was based on COI data only. All 16S rRNA sequences of specimens originating from the warm-temperate province were identical and distinct from the sequences of specimens from other regions, which supports their monophyly. Discussion Despite the fact that P. peringueyi may disperse in a number of ways (larval drifting as well as adult walking, swimming and rafting) and despite its ubiquity (being present in both estuaries and the nearshore habitat), the phylogeographic patterns identified were similar to those of coastal invertebrates that lack active adult dispersal. Like the planktonic dispersers U. africana (Teske et al. 2006) and P. perna (Zardi et al. 2007), P. peringueyi is characterised by a genetic discontinuity on the South-East Coast, and like in these other two species, there is some overlap among regional lineages (two different lineages were present in the Mbhanyana Estuary). Most biogeographic studies have indicated that the break between the cool-temperate and warm-temperate provinces is located near Cape Point (e.g. Stephenson and Stephenson 1972, Emanuel et al. 1992, Whitfield 1994, Turpie et al. 2000). However, of the species for which phylogeographic information is available to date, only the isopod Exosphaeroma hylecoetes has an intraspecific break in this region (Figure 1). The same species has a second phylogeographic break near Cape Agulhas, and a break in this region has also been found in other coastal invertebrates (Evans et al. 2004, Teske et al. 2006). Although Bayesian inference recovered all of the P. peringueyi specimens collected west of Cape Agulhas as a monophyletic clade, it is clear that there is some differentiation between the samples collected east and west of Cape Point (Bot Estuary vs Langebaan, Groot Berg and Olifants). Both Cape Point and Cape Agulhas can thus be considered to be biogeographic breaks that are separating regional lineages of P. peringueyi. Despite the potentially high motility of P. peringueyi, the genetic data indicate that this species is not as efficient a disperser as coastal teleosts. Spawning migrations have been reported for a number of palaemonid shrimps (Siegfried 1980, Manent and Abella-Gutiérrez 2006) and some are able to swim against currents (Nakata 1987). However, even though adult palaemonid shrimps are capable of powerful swimming, employing quick tail beats that propel them backwards during escape from predators or feeding, they tend to be quickly exhausted (Thebault and Raffin 1991) and are thus unlikely to undergo long-distance migrations by swimming for extended periods of time. For that reason, they may be similarly affected by the structuring effects of environmental discontinuities as species that are not capable of active adult dispersal. The fact that the emigration of young adult P. peringueyi out of estuaries occurs mainly during the nocturnal ebb-tide (Emmerson 1983, Wooldridge 1991) indicates that, like many estuarine crustacean larvae, adults of this species also primarily make use of favourable currents to allow them to reach suitable habitats. In addition, the dependence of P. peringueyi on estuaries or tidal rock pools may drive genetic divergence among

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0.1 100/96/97

100/100/100 98/–/– 96/–/–

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Olifants Olifants Olifants Olifants Olifants Langebaan Langebaan Langebaan Groot Berg Groot Berg Groot Berg

Bot Bot Bot Gourits Keurbooms Swartkops Swartkops Swartkops Gqunube Gqunube Qora Qora 100/100/100 Qora Mbhanyana Mbhanyana Keurbooms Gqunube Gourits Gourits –/100/100 Keurbooms Mngazana Mngazana Mbhanyana Mngazana Mngazana Mngazana 100/100/100 Mngazana Mngazana Mzimvubu Mzimvubu Mzimvubu Palaemon longirostris Macrobrachium nipponense

Cool-temperate

Warm-temperate

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Figure 2: A phylogram from Bayesian inference reconstructed from combined mtDNA COI and 16S rRNA sequences of Palaemon peringueyi. Numbers next to some clades are nodal support values from three methods of phylogenetic reconstruction: posterior probabilities (>95%) from Bayesian inference; bootstrap values (>75%) from neighbour-joining; and bootstrap values (>75%) from parsimony analysis. Clades are grouped on the basis of their association with South African marine biogeographic provinces

regional lineages. McMillen-Jackson and Bert (2003) studied two penaeid prawns that occupy different adult habitats, but are sympatric in estuaries as juveniles. They found strong geographic structure in the estuarine-dependent inshore species Litopenaeus setiferus and no structure in the offshore species Farfantepenaeus aztecus. This difference was attributed to the fact that L. setiferus lives in an unstable habitat and is prone to fluctuations in population sizes, which may result in temporarily lower effective population sizes and a greater probability of stochastic changes

in gene frequencies. The same may apply to P. peringueyi; as this species is unable to survive in water of low salinity, mortalities may occur in estuarine populations during freshwater floods (Allan et al. 2006). However, such fluctuations in population size mostly affect young individuals, whereas adults of spawning age often occur in more stable habitat in deeper water (<45m; Barnard 1950). An additional explanation for the large amount of genetic structure identified is that regional divergence may be driven by behavioural strategies. Vertical movement has

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been reported in a number of crustacean species (Shanks 1986, Peterson 1998, Queiroga and Blanton 2004) and presents a way of enhancing retention of larvae (MartaAlmeida et al. 2006). All larval stages of P. peringueyi have been found in plankton tows in the nearshore region of Algoa Bay on South Africa’s south coast (Emmerson 1986), but it is not known whether these undergo vertical migrations. Although research on the genetic structure of coastal invertebrates within marine biogeographic provinces in South Africa indicates that retention strategies do not result in significant isolation by distance among populations of species with planktonic larvae (Teske et al. in press b), they may nonetheless be an important mechanism driving genetic divergence between populations present in the different provinces when coupled with diversifying selection. Acknowledgements — This is a contribution from the African Coelacanth Ecosystem Programme. We are grateful to Martin Thiel for providing information on rafting as a means of dispersal in shrimps, to Isabelle Papadopoulos for advice on larval dispersal and retention, and to Charles Griffiths and George Branch for information about the distribution of Palaemon peringueyi. This study was supported by a Postdoctoral Research Fellowship from the Claude Harris Leon Foundation awarded to PRT, the National Research Foundation and Rhodes University.

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