The Synthesium Brachycladiidae Odhner, 1905 (Digenea) association with hosts based on nuclear and mitochondrial genes

doi:10.1016/j.parint.2011.08.008

Parasitology International

Volume 60, Issue 4, December 2011, Pages 530-533

https://doi.org/10.1016/j.parint.2011.08.008 Get rights and content

Abstract

Synthesium pontoporiae, exclusive parasite of the endangered dolphin, Pontoporia blainvillei, is endemic and restricted to the South Atlantic and belongs to the Brachycladiidae family Odhner, 1905. The study of this family has been limited by the difficulty of accessing the parasites from their marine mammal hosts and as a consequence there is a paucity of genetic information available. Herein we present a genetic analysis using 18S rDNA sequences of S. pontoporiae and S. tursionis and the ND3 mtDNA sequence of S. pontoporiae. The genetic analysis of 18S rDNA sequences of brachycladiids and acanthocolpids determined two major clusters associated with their definitive hosts, marine mammals and fishes, respectively. Considering the tree topology of brachycladiids ND3 mtDNA gene, two clusters were defined, one with the Synthesium species. This work contributes with fundamental genetic information on S. pontoporiae, and suggests a Brachycladiidae genetic evolution related to their hosts.

Graphical abstract

Highlights

► New taxonomic information of Synthesium pontoporiae and S. tursionis Brachycladiidae (Digenea). ► New molecular data for these species based on two molecular markers: the 18S rDNA and ND3 mtDNA gene. ► The establishment of the Synthesium position among the Brachycladiidae. ► Evidence of associations between different digeneans and the site of infection.

Section snippets

Acknowledgements

This work is part of the PhD Dissertation of J. Marigo. This work was sponsored by the LGMM-IOC grant, PAPES V-FIOCRUZ, CAPES, CNPq and FAPERJ. We thank Koko Otsuki and Fernanda Freitas for their technical assistance. Heloisa M. Diniz (Laboratório de Produção e Tratamento de Imagem-IOC) for graphic assistance and PDTIS/FIOCRUZ genomic platform for DNA sequencing.

References (19)

T.H.C. Cribb et al.
Life cycle evolution in the Digenea: a new perspective from phylogeny
Adv Parasitol
(2003)
P.D. Olson et al.
Advances and trends in the molecular systematics of the parasitic Platyhelminthes
Adv Parasitol
(2005)
D.W. Liu et al.
The nucleotide sequence and predicted secondary structure of small subunit (18S) ribosomal RNA from Spirometra erinaceieuropaei
Gene
(1997)
A.M. Iñiguez et al.
Genetic characterization of Anisakis typica and Anisakis physeteris from marine mammals and fish from the Atlantic Ocean off Brazil
Vet Parasitol
(2009)
M. Dorris et al.
The small subunit ribosomal RNA sequence of Strongyloides stercoralis
Int J Parasitol
(2000)
P.D. Olson et al.
Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda)
Int J Parasitol
(2003)
T.H. Cribb et al.
Diversity in the Monogenea and Digenea: does lifestyle matter?
Int J Parasitol
(2002)
N.B. Chilton et al.
The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts
Mol Phylogenet Evol
(2006)
M.C. Durette-Desset et al.
The origins and evolutionary expansion of the Strongylida (Nematoda)
Int J Parasitol
(1994)

There are more references available in the full text version of this article.

Cited by (9)

Macroparasites of franciscana: what can their coexistence say to conservationists?
2022, The Franciscana Dolphin: On the Edge of Survival
The helminth assemblage of franciscana is apparently predictable and depauperate due to its evolutionary process, feeding habits, and its localized habitat use. The gastrointestinal tract of franciscana harbor the majority of these parasites and these species have been recorded: Synthesium pontoporiae (Digenea: Brachycladiidae), Corynosoma cetaceum, Bolbosoma turbinela (Acanthocephala: Polymorphidae), Anisakis typica, and A. simplex (Nematoda: Anisakidae). Synthesium pontoporiae and C. cetaceum are the most important species, showing the higher infection levels in this host. Both have been also indicated as biological tags to investigate the existence of stocks of franciscana since they are easy to collect, show no lethal effect, and their infection levels express an evident increasing tendency toward southern areas. A standardized methodology for helminth collection and the use of recognized parameters to evaluate infection levels are recommended.
The biodiversity of marine trematodes: then, now and in the future
2021, International Journal for Parasitology
Citation Excerpt :
We suspect that a component of the diminution in description of trematodes of marine tetrapods relates simply to the difficulty in obtaining samples. In this context we here express our admiration for the body of recent work relating to the brachycladiids of marine mammals (Marigo et al., 2008; Marigo et al., 2011; Fraija-Fernandez et al., 2015, 2016; Kremnev et al., 2020). Deletion of the trematodes of tetrapods from the data set produces an accumulation curve for fish trematodes that shows fewer signs of a plateau than that for those of marine tetrapods (Fig. 2E).
Trematodes are the richest class of platyhelminths in the marine environment, infecting all classes of marine vertebrates as sexual adults and many phyla of marine invertebrates as part of their life cycles. Despite the cryptic nature of their existence (almost all marine trematodes are internal parasites), they have been the focus of study for almost 250 years, with the first species described in 1774. Here we review progress in the study of the “biodiversity” of these parasites, contrasting the progress made in the last 50 years (post-1971) to that in the almost 200 years before it (pre-1972). We consider an understanding of biodiversity to require knowledge of the species present in the system, an understanding of their evolutionary relationships (which informs higher classification), and, specifically for trematodes, an understanding of their complex life cycles. The fauna is now large, comprising well over 5,000 species. Although species description continues, we see evidence of a slow-down in all aspects of discovery. There has been only one completely new family identified since 1984 and the proposal of new genera is in decline as is the description of new species, especially for those of tetrapods. However, the extent to which this slow-down reflects an approach to the richness asymptote is made uncertain by changes in the field; reduced effort and difficulty of study may be important components of the effect. Regardless of how close we are to a complete description of the fauna, we infer that the outline is well-understood although the details are not. Adoption of molecular methodologies over the last 40 years have complemented morphometric analyses to facilitate objective recognition of species; however, despite these objective data, there is still inconsistency between authors on species delimitation. Molecular methodologies have also completely revolutionised inference of relationships at all levels, from within genera to between orders, and underpinned elucidation of novel life cycles. We expect the next 50 years to produce further dividends from technological innovations. The backdrop to the field will be global environmental concerns and the growing problem of funding for basic biodiversity studies.
Evolutionary relationships between digeneans of the family Brachycladiidae Odhner, 1905 and their marine mammal hosts: A cophylogenetic study
2016, Parasitology International
Citation Excerpt :
The fact that brachycladiids are trophically-transmitted parasites that presumably exploit food webs extensively may have provided opportunities for colonization of new, unrelated hosts, during their evolution. Previous studies on the Brachycladiidae have analysed partial phylogenetic relationships within the family, suggesting hypotheses about their origin and diversification [24–27]. Brachycladiids likely originated through a host-switching event, when their ancestor, having marine fish as former definitive hosts, was able to shift to odontocetes through predator–prey relationships [24,28].
Cophylogenetic studies examine the congruence between host and parasite phylogenies. There are few studies that quantify the relative contribution of coevolutionary events, i.e. duplication, loss, failure-to-diverge, host-switching and spreading in trophically-transmitted parasites at the marine realm. We addressed this issue in the Brachycladiidae, a cosmopolitan digenean family specific to marine mammals. We used, for the first time, distance-based and event-based methods to explicitly test the coevolutionary events that have shaped the current brachycladiid-marine mammal associations. Parasite phylogeny was constructed using mtDNA ND3 sequences of nine brachycladiid species, and host phylogeny using cytochrome b sequences of 104 mammalian species. A total of 50 host-parasite links were identified. Distance-based methods supported the hypothesis of a global non-random association of host and parasite phylogenies. Significant individual links (i.e., 24 out of 50) were those related to Campula oblonga, Nasitrema delphini, N. globicephalae and Brachycladium atlanticum and their associated taxa from the Delphinoidea. Regarding event-based methods, we explored 54 schemes using different combinations of costs for each potential coevolutionary event. Three coevolutionary scenarios were identified across all schemes and in all cases the number of loss events (87–156) was the most numerous, followed by failure-to-diverge (40), duplication (3–6), host-switching (0–3) and cospeciation (0–2). We developed a framework to interpret the evolution of this host-parasite system and confirmed that failure-to-diverge and colonization with or without subsequent diversification could have been decisive in the establishment of the associations between brachycladiids and marine mammals.
Molecular identification of the strongyloid nematode Oesophagostomum aculeatum in the Asian wild elephant Elephas maximus
2016, Journal of Helminthology
Genetic diversity and population structure of Synthesium pontoporiae (Digenea, Brachycladiidae) linked to its definitive host stocks, the endangered Franciscana dolphin, Pontoporia blainvillei (Pontoporiidae) off the coast of Brazil and Argentina
2015, Journal of Helminthology
MORPHOLOGICAL AND MOLECULAR CHARACTERIZATION OF OESPHAGOSTOMUM COLUMBIANUM IN GOAT AT LUCKNOW DISTRICT, UTTAR PRADESH
2020, Biochemical and Cellular Archives

View all citing articles on Scopus

View full text

Article preview

Parasitology International

Abstract

Graphical abstract

Highlights

Section snippets

Acknowledgements

References (19)

Life cycle evolution in the Digenea: a new perspective from phylogeny

Adv Parasitol

Advances and trends in the molecular systematics of the parasitic Platyhelminthes

Adv Parasitol

The nucleotide sequence and predicted secondary structure of small subunit (18S) ribosomal RNA from Spirometra erinaceieuropaei

Gene

Genetic characterization of Anisakis typica and Anisakis physeteris from marine mammals and fish from the Atlantic Ocean off Brazil

Vet Parasitol

The small subunit ribosomal RNA sequence of Strongyloides stercoralis

Int J Parasitol

Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda)

Int J Parasitol

Diversity in the Monogenea and Digenea: does lifestyle matter?

Int J Parasitol

The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts

Mol Phylogenet Evol

The origins and evolutionary expansion of the Strongylida (Nematoda)

Int J Parasitol

Cited by (9)

Macroparasites of franciscana: what can their coexistence say to conservationists?

The biodiversity of marine trematodes: then, now and in the future

Evolutionary relationships between digeneans of the family Brachycladiidae Odhner, 1905 and their marine mammal hosts: A cophylogenetic study

Molecular identification of the strongyloid nematode Oesophagostomum aculeatum in the Asian wild elephant Elephas maximus

Genetic diversity and population structure of Synthesium pontoporiae (Digenea, Brachycladiidae) linked to its definitive host stocks, the endangered Franciscana dolphin, Pontoporia blainvillei (Pontoporiidae) off the coast of Brazil and Argentina

MORPHOLOGICAL AND MOLECULAR CHARACTERIZATION OF OESPHAGOSTOMUM COLUMBIANUM IN GOAT AT LUCKNOW DISTRICT, UTTAR PRADESH

Short communicationThe Synthesium Brachycladiidae Odhner, 1905 (Digenea) association with hosts based on nuclear and mitochondrial genes

Abstract

Graphical abstract

Highlights

Section snippets

Acknowledgements

Adv Parasitol

Adv Parasitol

Gene

Vet Parasitol

Int J Parasitol

Int J Parasitol

Int J Parasitol

Mol Phylogenet Evol

Int J Parasitol

Short communication
The Synthesium Brachycladiidae Odhner, 1905 (Digenea) association with hosts based on nuclear and mitochondrial genes