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The Phylogeny and Life Cycle of Two Species of Profilicollis (Acanthocephala: Polymorphidae) in Marine Hosts Off the Pacific Coast of Chile

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The Phylogeny and Life Cycle of Two Species of Profilicollis (Acanthocephala: Polymorphidae) in Marine Hosts Off the Pacific Coast of Chile Journal of Helminthology, Page 1 of 8 doi:10.1017/S0022149X16000638 © Cambridge University Press 2016 The phylogeny and life cycle of two species of Profilicollis (Acanthocephala: Polymorphidae) in marine hosts off the Pacific coast of Chile S.M. Rodríguez1*, G. D’Elía2 and N. Valdivia1,3 1Doctorado en Biología Marina and Instituto de Ciencias Marinas y Limnológicas, Facultad de Ciencias, Universidad Austral de Chile, campus Isla Teja s/n, Valdivia, Chile: 2Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile: 3Centro FONDAP de Investigación en Dinámica de Ecosistemas Marinos de Altas Latitudes (IDEAL) (Received 7 June 2016; Accepted 20 August 2016) Abstract Resolving complex life cycles of parasites is a major goal of parasitological re- search. The aim of this study was to analyse the life cycle of two species of the genus Profilicollis, the taxonomy of which is still unstable and life cycles unclear. We extracted individuals of Profilicollis from two species of crustaceans (inter- mediate hosts) and four species of seagulls (definitive hosts) from sandy-shore and estuarine habitats along the south-east Pacific coast of Chile. Mitochondrial DNA analyses showed that two species of Profilicollis infected intermediate hosts from segregated habitats: while P. altmani larvae infected ex- clusively molecrabs of the genus Emerita from fully marine habitats, P. antarcticus larvae infected the crab Hemigrapsus crenulatus from estuarine habitats. Moreover, P. altmani completed its life cycle in four seagulls, Chroicocephalus ma- culipennis, Leucopheus pipixcan, Larus modestus and L. dominicanus, while P. antarc- ticus, on the other hand, completed its life cycle in the kelp gull L. dominicanus. Accordingly, our results show that two congeneric parasites use different and spatially segregated species as intermediate hosts, and both are capable of infect- ing one species of definitive hosts. As such, our analyses allow us to shed light on a complex interaction network. Introduction 2010), and a single parasite species can have multiple intermediate and definitive host species (Near, 2002; One of the major goals of parasitological research is to Mayer et al., 2003; Royal et al., 2004; La Sala & clarify the life cycles of parasites. Most of these parasites Martorelli, 2007; Steinauer et al., 2007; Kochin et al., have complex life cycles, being trophically transmitted be- 2010; La Sala et al., 2013). tween intermediate and definitive hosts (Thomas et al., Parasites of the genus Profilicollis (Polymorphidae: 2009; Thieltges et al., 2013). Although the evolution of Acanthocephala) infect marine mammals, shorebirds parasites and that of hosts are not independent of each and waterfowl as definitive hosts, and amphipods, deca- other, parasites can evolve far more rapidly than hosts pods and euphausiids as intermediate hosts (Balboa (Kochin et al., 2010). As a consequence, parasites can et al., 2009; García-Varela et al., 2013). In the definitive switch hosts in a given environment (Kochin et al., predator host, the adult female worm develops and pro- duces eggs (acanthors) that are released into the environ- ment through the host faeces. Upon its intake by an *E-mail: [email protected] arthropod host, the acanthor develops in the haemocoele Downloaded from http:/www.cambridge.org/core. Tufts Univ, on 27 Sep 2016 at 22:44:30, subject to the Cambridge Core terms of use, available at http:/www.cambridge.org/core/terms. http://dx.doi.org/10.1017/S0022149X16000638 2 S.M. Rodríguez et al. into an acanthellae and then into a cystacanth. Finally, the We analysed molecular data in order to identify accurate- cystacanth infects the definitive host when the latter pre- ly acanthocephalan specimens collected from intermedi- dates upon an infected intermediate prey host ate and definitive hosts along 1200 km of the Chilean SE (Zdzitowiecki, 1985). Pacific coast. Two Profilicollis species have been described from the shores of the south-east (SE) Pacific (Amin, 2013) – P. alt- mani (Perry, 1942; = P. bullocki Mateo, 1982) and P. antarc- Materials and methods – ticus Zdzitowiecki, 1985 which infect intermediate hosts Collection and examination of crab and avian hosts from segregated habitats with little or no spatial overlap. While P. altmani infects the sandy-shore molecrab Emerita The study area corresponded to marine and estuarine analoga (Stimpson, 1857) (Goulding & Cohen, 2014; systems along the SE Pacific coast of Chile. Sandy-shore Rodríguez & D’Elía, 2016), P. antarcticus infects the estuar- molecrabs, estuarine crabs and seagulls were captured at ine crab Hemigrapsus crenulatus (Varunidae; Milne- six sites located between 29.9 and 39.5°S, spanning Edward, 1837) (Haye & Ojeda, 1998; Latham & Poulin, 1200 km of the shore. The sandy beaches surveyed were 2002a). However, recent work challenges the identifica- ‘Coquimbo’ (29.9°S–71.2°W), ‘Dichato’ (36.4°S–72.9°W), tion of the Profilicollis species that infects H. crenulatus, ‘Colcura’ (37.1°S–73.1°W), ‘Calfuco’ (39.7°S–73.3°W) and which has been ascribed either to P. antarcticus or another ‘Chaihuín’ (39.9°S−73.5°W). The estuarine site corre- species, namely P. chasmagnathi (Balboa et al., 2009). sponded to the mouth of the Valdivia River, ‘Niebla’ Therefore, it is still unclear which species actually infects (39.8°S–73.4°W). the estuarine crab H. crenulatus. In the sandy-shore sites, 239 individuals of the mole- In addition to the unclear parasite–intermediate host link crab E. analoga were captured during 2014 and 2015 in described above, the identity of the species of Profilicollis in- winter and summer seasons. At each site and sampling fecting the definitive hosts is also unclear. While P. antarcti- time, four transects were randomly deployed perpendicu- cus has been registered only as a parasite of the kelp gull larly to the shoreline. Along each transect we placed Larus dominicanus (Lichtenstein, 1823) (Torres et al., 1991, six sampling stations located c. 2 m apart from each Latham & Poulin, 2002b), P. altmani has been described in other, from the effluent line to the swash line. Plastic 2 that seabird in addition to Chroicocephalus maculipennis corers (0.03 m ) were buried to a depth of 20 cm and the Lichtenstein, 1823, Leucopheus pipixcan (Wagler, 1831), sand was sieved through a 1-mm-mesh sieve. Crabs Podiceps sp. and Numenius phaeopus (Linnaeus, 1758). were transferred to the laboratory for parasite identifica- However, significant morphological differences between P. tion and sorting. In the estuarine site, 30 individuals of altmani individuals collected from different seabird species H. crenulatus were sampled by hand between October have been found (Riquelme et al., 2006), suggesting that 2015 and March 2016 along a 300-m transect on promon- these individuals might belong to more than one species. tory rocks. In order to answer the question of which parasite spe- A total of 16 seagulls were captured around 40°S on the cies (co-)occur in this parasitic system, we can suggest SE Pacific coast. Specimens were captured in resting areas that, due to the differences in the prey item consumption by means of a 3 × 5 m Whosh net trap installed in the and high mobility of seagulls (Smith, 2007; Yorio et al., morning and activated after 2 h. After capture, the speci- −1 2013), both Profilicollis species could be found co- mens were sedated with 40 mg kg of ketamine plus −1 occurring in any of the definite hosts. On the other 7mgkg of xylazine and transferred to the laboratory. hand, intermediate host species occur in specific habitats In addition, we analysed nine seagulls found dead during and with little spatial overlap (i.e. molecrabs inhabiting March–April 2015 and summer of 2016 in the sampling re- full marine habitats and crabs inhabiting estuaries), gion around 40°S. In summary, the analysed seagull sam- which can stimulate specific and strict parasite–intermedi- ple was as follows: C. maculipennis (n = 8), L. dominicanus ate host relationships (Near, 2002; Steinauer et al., 2007). (n = 8), L. modestus (n = 8) and L. pipixcan (n = 1). Thus, we might expect parasite co-occurrence in defini- Each sampled crustacean was dissected, and the abun- tive, but not in intermediate, hosts. Testing this hypothesis dance of Profilicollis spp. in the haemocoele was determined requires the accurate identification of parasite species. Up under a stereomicroscope. Seagulls were euthanized using −1 to now, the identification of these species has been almost an overdose of 0.2–1mlkg intracardiac thiopental. exclusively based on morphological characters. The ana- Afterwards, the birds were necropsied and each gastro- lysis of this type of evidence has provided valuable contri- intestinal tract was removed and opened in order to sort, butions to our understanding of parasite–host interactions, identify and count the Profilicollis parasite specimens. but its reliability can be severely compromised by the high Parasites were identified on the basis of published morpho- morphological similarity among acanthocephalan species logical characters (e.g. Riquelme et al., 2006;Balboaet al., (Near et al., 1998,Balboaet al., 2009)andthescarceknowl- 2009). A total of 749 Profilicollis specimens were extracted edge of their geographic variation. Therefore, the assess- from the different hosts (see table 1) and were stored in ment of molecular data provides an opportunity to 95% ethanol for subsequent DNA extraction. Prevalence identify cryptic species accurately (e.g. Goulding & and intensity of infection in each host species were calcu- Cohen, 2014; Rodríguez & D’Elía, 2016), and can well be lated according to Bush et al.(1997). used to shed light on the potentially complex Profilicollis interaction network in SE Pacific shores. Molecular and phylogenetic analyses Here, we test whether multiple Profilicollis species are able to co-occur in definitive (seagulls) and intermediate Genetic analyses were based on a fragment of 578 bp of (marine and estuarine crabs) hosts in SE Pacific shores. the mitochondrial cytochrome oxidase I (COI) gene.
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