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Taxonomic and Molecular Assessment of the Apparently Alien and Cosmopolitan Nereididae Blainville, 1818 Polychaetes from South Africa

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Taxonomic and Molecular Assessment of the Apparently Alien and Cosmopolitan Nereididae Blainville, 1818 Polychaetes from South Africa Taxonomic and molecular assessment of the apparently alien and cosmopolitan Nereididae Blainville, 1818 polychaetes from South Africa Jyothi Kara Dissertation presented for the Degree of Doctor of Philosophy in the Faculty of Science at Stellenbosch University Supervisor: Dr Carol A. Simon Co-supervisors: Dr Angus H.H Macdonald and Dr Kerry Sink April 2019 Stellenbosch University https://scholar.sun.ac.za Declaration By submitting this dissertation electronically, I declare that the entirety of the work contained therein is my own, original work, that I am the sole author thereof (save to the extent explicitly otherwise stated), that reproduction and publication thereof by Stellenbosch University will not infringe any third party rights and that I have not previously in its entirety or in part submitted it for obtaining any qualification. This dissertation includes one original paper published in a peer-reviewed journal and three unpublished publications. The collection, processing and analysis of data and writing of the papers (published and unpublished) were the principal responsibility of myself whereas Dr Carol Simon and Dr Angus Macdonalad were responsible for editing of the manuscripts thereafter. Jyothi Kara Copyright © 2019 Stellenbosch University All rights reserved i Stellenbosch University https://scholar.sun.ac.za Abstract Polychaete worms provide many ecosystem services and are useful indicator species. Some are invasive and may threaten biodiversity and ocean economies. However, the convoluted taxonomic history of polychaetes has led to incorrect classifications of indigenous and alien species as they are commonly mistaken for cosmopolitan species. Thus, species with a dubious taxonomic status are termed pseudocosmopolitan species. Three such species, Pseudonereis variegata Grube, 1857, Platynereis dumerilii Audouin & Milne Edwards, 1833 and Platynereis australis Schmarda, 1861 were prioritised for investigation owing to their alien or cryptogenic status elsewhere, multiple synonymised names, globally disjunct distribution and a widespread South African distribution. The first overarching aim of this thesis was to determine whether these three species are indigenous or alien to South Africa or harbour cryptic and new species. Thorough morphological revisions and molecular datasets (mtCOI and nDNA) revealed that all three species are indigenous to South Africa. The local Pseudonereis podocirra n. comb. (Schmarda, 1861) was incorrectly synonymised as P. variegata (type locality: Chile) and Platynereis B sp. nov. was misidentified as P. dumerilii (type locality: Mediterranean). Individuals identified as P. australis (type locality: New Zealand) represent P. massiliensis (Moquin-Tandon, 1869) (type locality: Mediterranean), but since individuals from Italy and Portugal nested within the South African clade and had comparatively low genetic diversities, this species is likely indigenous to South Africa and alien in the Mediterranean. However, because P. massiliensis is part of a cryptic species complex in the Mediterranean, its name is considered doubtful and hence is referred to as P. massiliensis s.l. Pseudonereis podocirra’s wrongful synonymisation was due to poor species descriptions and conservative taxonomic views whereas misidentifications of the two Platynereis species was because they are truly cryptic. These results together with the finding that ~50% of other local nereidids may be pseudocosmopolitan, indicate that diversity of nereidids has been underestimated. Short-term solutions are proposed when dealing with pseudocosmopolitan polychaete species and recommendations are made regarding the clarification of P. massiliensis s.l. in the Mediterranean, the molecular identification of the global Platynereis species complex and taxonomic revisions of P. variegata from Chile. The second overarching aim was to determine factors contributing to the phylogeographic structure of these three ii Stellenbosch University https://scholar.sun.ac.za sympatric South African species to determine the underlying factors driving their present-day distributions. Using mtCOI, P. massiliensis s.l. displayed three geographically structured lineages separated by the Cape Point and Cape Agulhas phylogeographic breaks whereas Platynereis B sp. nov. showed two well-mixed regional lineages separated by the Cape Agulhas break. In contrast, nDNA demonstrated well-mixed populations for both species and the intrinsic properties of each marker was used to explain the differences in patterns. Pseudonereis podocirra exhibited a panmictic meta-population using a mitochondrial dataset which persisted even when using a high-throughput SNP dataset. Age, hence resilience, were likely factors contributing to the contrasting patterns of structure and connectivity as P. podocirra n. comb. was demonstrated to be an evolutionarily older species. Fluctuating temperatures and paleo-conditions during the Pleistocene probably resulted in the southeastern expansions of all three species while radiations along the west coast were inferred for Platynereis B sp. nov. and P. podocirra. Platynereis B sp. nov. and P. massiliensis s.l. speciated sympatrically due to reproductive isolation and temperature, whereas P. massiliensis s.l. and P. dumerilii are hypothesised to have speciated allopatrically. All Platynereis species display evidence of morphological stasis despite their ancient divergence times. Pseudonereis podocirra and P. variegata (Chile) speciated allopatrically and have undergone morphological stasis or convergence. Historical climatic oscillations, oceanographic currents, ecoregions and larval development were factors contributing to the phylogeographic structure whilst allopatry and sympatry coupled with morphological stasis were identified as the most likely mode and mechanism of cryptic speciation of these species in South Africa. iii Stellenbosch University https://scholar.sun.ac.za Opsomming Borselwurms verteenwoordig ‘n groot deel van seebodem habitat diversiteit en verskaf vele ekosisteem dienste insluitend voedingstof hersirkulasie en habitat voorsiening. Baie is indringer- spesies en kan die plaaslike diversiteit en mariene-ekonomie bedreig. Bygesê, die ingewikkelde taksonomiese geskiedenis van borselwurms het gelei tot die inkorrekte klassifikasie van inheemse en indringer spesies deur hul as wydverspreide of kosmopolitiese spesies te klassifiseer. Dus, spesies met ‘n twyfelagtige taksonomiese status word pseudo-komopolitaanse spesies genoem. Drie sulke spesies, Pseudonereis variegata Grube, 1857, Platynereis dumerilii Audouin & Milne Edwards, 1833 en Platynereis australis Schmarda, 1861 is as prioriteit beskou vir verdere ondersoek namate hul status as indringer-, twyfelagtige- of kriptogeniese- spesies elders, asook verskeie sinonomiese name, gebroke globale verspreiding en wydverspreide Suid-Afrikaanse verspreiding. Die eerste oorkoepelende doelwit was om vas te stel of hierdie Suid-Afrikaanse spesies wel inheems tot die streek is. Deeglike morfologiese wysigings en molekulêre datastelle (mtCOI en nDNS) het al drie spesies as inheems openbaar. Die plaaslike Pseudonereis podocirra n. comb. (Schmarda, 1861) is inkorrek as sinoniem van P. variegata (tipe ligging: Chile) aangedui en Platynereis B sp. nov. was verkeerdelik identifiseer as P. dumerilii (tipe ligging: Mediterreens). Individue identifiseer as P. australis (tipe ligging: Nieu-Seeland) verteenwoordig P. massiliensis (Moquin-Tandon, 1869) (tipe ligging: Mediterreens), maar sedert individue van Italië en Portugal geneste is binne die Suid- Afrikaanse klade en vergelykend lae genetiese diversiteit gehad het is daar tot die gevolgtrekking gekom dat hierdie spesie inheems tot Suid-Afrika is en ‘n indringer spesie in die Mediterreense see is. Omdat P. massiliensis deel vorm van n kriptiese spesie-kompleks in die Mediterreense see word die naam as twyfelagtig beskou en word dus voortaan verwys na “P. massiliensis”. Die verkeerdelike sinonomie van Pseudonereis podocirra was as gevolg van onvoldoende spesie beskryfwings asook die konservatiewe uitsigte van taksonomiese kenners terwyl die verkeerdelike identifikasie van die twee Platynereis spesies plaasgevind het as gevolg van hul kriptiese morfologie. Hierdie resultate tesame met die vinding dat ~50% van ander plaaslike nereidid spesies pseudo-kosmopolitaans kan wees is beduidend daarop dat die diversiteit van nereidid speies onderskat is. Kort-termyn oplossings word voorgestel vir die hantering van pseudo-kosmopolitaanse spesies en aanbevelings iv Stellenbosch University https://scholar.sun.ac.za word gemaak met betrekking tot die klassifikasie van “P. massiliensis” in die Mediterreense see, die molekulêre identifikasie van die globale Platynereis spesie kompleks en taksonomiese wysigings van P. variegate van Chile. Die tweede oorkoepelende doelwit was om vas te stel watter faktore bydrae tot die filo-geografiese strukture van die drie simpatriese Suid-Afrikaanse spesies om sodoende die onderliggende faktore wat hedendaagse verspreiding dryf vas te stel. Met mtCOI het “P. massiliensis” drie geografies gestruktureerde bevolkings gehad wat geskei is by die Kaapse Punt en Kaap Agullhas filo-geoagrafiese breuke terwyl Platynereis B sp. nov. net twee goed gemengde plaaslike afstammelinge aandui wat geskei is by die Kaap Agullhas breuk. In kontras het die nDNS goed gemengde bevolkings aangedui vir beide spesies en die intrinsieke eieskappe van elke merker is gebruik om die verskille in patrone te verduidelik. Pseudonereis podocirra het
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