Molecular systematics of pinniped hookworms (Nematoda: Uncinaria): species delimitation, host associations and host-induced morphometric variation

Abstract

a b s t r a c tHookworms of the genus Uncinaria have been widely reported from juvenile pinnipeds, however investigations of their systematics has been limited, with only two species described, Uncinaria lucasi from northern fur seals (Callorhinus ursinus) and Uncinaria hamiltoni from South American sea lions (Otaria flavescens). Hookworms were sampled from these hosts and seven additional species including Steller sea lions (Eumetopias jubatus), California sea lions (Zalophus californianus), South American fur seals (Arctocephalus australis), Australian fur seals (Arctocephalus pusillus), New Zealand sea lions (Phocarctos hookeri), southern elephant seals (Mirounga leonina), and the Mediterranean monk seal (Monachus monachus). One hundred and thirteen individual hookworms, including an outgroup species, were sequenced for four genes representing two loci (nuclear ribosomal DNA and mitochondrial DNA). Phylogenetic analyses of these sequences recovered seven independent evolutionary lineages or species, including the described species and five undescribed species. The molecular evidence shows that U. lucasi parasitises both C. ursinus and E. jubatus, whereas U. hamiltoni parasitises O. flavescens and A. australis. The five undescribed hookworm species were each associated with single host species (Z. californianus, A. pusillus, P. hookeri, M. leonina and M. monachus). For parasites of otarids, patterns of Uncinaria host-sharing and phylogenetic relationships had a strong biogeographic component with separate clades of parasites from northern versus southern hemisphere hosts. Comparison of phylogenies for these hookworms and their hosts suggests that the association of U. lucasi with northern fur seals results from a host-switch from Steller sea lions. Morphometric data for U. lucasi shows marked host-associated size differences for both sexes, with U. lucasi individuals from E. jubatus significantly larger. This result suggests that adult growth of U. lucasi is reduced within the host species representing the more recent hostparasite association. Intraspecific host-induced size differences are inconsistent with the exclusive use of morphometrics to delimit and diagnose species of Uncinaria from pinnipeds.

Parasitological examination of northern elephant seal (Mirounga angustirostris) pups for presence of hookworms (Uncinariaspp.) on San Miguel Island, California

“…Southern elephant seals were exploited but the population apparently was not reduced to numbers as low as NESs. The specifi city of hookworms to their pinniped hosts has repeatedly been suggested (George-Nascimento et al, 1992;Nadler et al, 2013;Ramos et al, 2013). Twelve species of Uncinaria which signifi cantly differ both morphologically and according to molecular studies were described in pinnipeds (Castinel et al, 2006;Nadler et al, 2013;Ramos et al, 2013).…”

“…This allowed NESs, because of the sympatric relationship with the aforementioned pinnipeds, to get infected by these parasitic nematodes; however this did not happen. Hookworms in the genus Uncinaria have been found in several species of pinnipeds from different regions of the world (Lyons et al, 2011;Nadler et al, 2013;Dailey, 2001), that lead to the interest in trying to fi nd if these parasites are present in NESs. However, despite extensive studies of NES pups and the environment performed in 2012 on the Año Nuevo State Reserve (Lyons et al, 2012), in examination of NES pups from TMMC and in the present study on San Miguel Island, evidence of Uncinaria parasitizing this species of pinnipeds has not been found.…”

“…Hookworms from the genus Uncinaria Frölich, 1789 have been reported in 15 pinniped species -12 otariids (six species of fur seals, and six species of sea lions) and three phocids (Lyons et al, 2011;Nadler et al, 2013). Four species of hookworms have been described in pinnipeds -Uncinaria lucasi Stiles, 1901, a parasite of northern fur seals (NFSs) (Callorhinus ursinus) and Steller sea lions (Eumetopias jubatus); Uncinaria hamiltoni Baylis, 1933, a parasite of South American sea lions (Otaria flavescens) and South American fur seals (Arctocephalus australis); Uncinaria sanguinis Marcus, Higgins, Šlapeta, Gray 2014, a parasite of Australian sea lions (Neophoca cinerea) and, probably, Australian fur seals (Arctocephalus pusillus) and New Zealand fur seals (Arctocephalus forsteri) (Marcus et al, 2014); Uncinaria lyonsi Kuzmina and Kuzmin 2015, a parasite of California sea lions (CSLs) (Zalophus californianus).…”

“…Four species of hookworms have been described in pinnipeds -Uncinaria lucasi Stiles, 1901, a parasite of northern fur seals (NFSs) (Callorhinus ursinus) and Steller sea lions (Eumetopias jubatus); Uncinaria hamiltoni Baylis, 1933, a parasite of South American sea lions (Otaria flavescens) and South American fur seals (Arctocephalus australis); Uncinaria sanguinis Marcus, Higgins, Šlapeta, Gray 2014, a parasite of Australian sea lions (Neophoca cinerea) and, probably, Australian fur seals (Arctocephalus pusillus) and New Zealand fur seals (Arctocephalus forsteri) (Marcus et al, 2014); Uncinaria lyonsi Kuzmina and Kuzmin 2015, a parasite of California sea lions (CSLs) (Zalophus californianus). In addition, three species from the genus Uncinaria were found and determined from nucleotide sequence data in the New Zealand sea lion (Phocarctos hookeri), southern elephant seal (Mirounga leonina) and Mediterranean monk seal (Monachus monachus) (Castinel et al, 2006;Nadler et al, 2013;Ramos et al, 2013). Hookworms (Uncinaria spp.)…”

“…have also been reported from Juan Fernandez fur seal pups (Arctocephalus philippii) (Sepúlveda, 1998) and Guadaloupe fur seals (Arctocephalus townsendi) (Lyons et al, personal communication). From the family Phocidae (earless or true seals), hookworms were found only in the southern elephant seal, ringed seal (Phoca hispi-da) and Mediterranean monk seal (Lyons et al, 2011;Nadler et al, 2013). Despite the reference that hookworm eggs were detected in feces of a northern elephant seal (NES) (Mirounga angustirostris) pup at The Marine Mammal Center (TMMC), Sausalito, California (Dailey, 2001), this information is still questionable.…”