The phylogenetic relationships and species richness of host-specific  Dactylogyrus  parasites shaped by the biogeography of Balkan cyprinids

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Abstract

Parasites exhibiting a high degree of host specificity are expected to be intimately associated with their hosts. Therefore, the evolution of host-specific parasites is at least partially shaped by the evolutionary history and distribution of such hosts. Gill ectoparasites of Dactylogyrus (Monogenea) are specific to cyprinid fish. In the present study, we investigated the evolutionary history of 47 Dactylogyrus species from the Balkan Peninsula, the Mediteranean region exhibiting the highest cyprinid diversity in Europe, and from central European cyprinids. Phylogenetic analyses revealed four well-supported clades of endemic and non-endemic Dactylogyrus spp. with four basal taxa. Endemic cyprinids with a limited distribution range were parasitized by endemic Dactylogyrus species, but some of them shared several Dactylogyrus species with central European cyprinids. Species delimitation analyses based on molecular data suggest that Dactylogyrus diversity is higher than that defined from morphology. Some endemic cyprinid species harboured Dactylogyrus species of different origins, this probably resulting from multiple host switching. Our results support the view that the evolution of Dactylogyrus in the Balkans has been influenced not only by the historical dispersion and distribution of their cyprinid hosts, but also by recent contacts of non-native cyprinid species with endemic cyprinid fauna in this region.

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Phylogenetic relationships and biogeographical patterns in Circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data

Silvia Perea, Madelaine Böhme, Primož Zupančič … (2010)

Background Leuciscinae is a subfamily belonging to the Cyprinidae fish family that is widely distributed in Circum-Mediterranean region. Many efforts have been carried out to deciphering the evolutionary history of this group. Thus, different biogeographical scenarios have tried to explain the colonization of Europe and Mediterranean area by cyprinids, such as the "north dispersal" or the "Lago Mare dispersal" models. Most recently, Pleistocene glaciations influenced the distribution of leuciscins, especially in North and Central Europe. Weighing up these biogeographical scenarios, this paper constitutes not only the first attempt at deciphering the mitochondrial and nuclear relationships of Mediterranean leuciscins but also a test of biogeographical hypotheses that could have determined the current distribution of Circum-Mediterranean leuciscins. Results A total of 4439 characters (mitochondrial + nuclear) from 321 individuals of 176 leuciscine species rendered a well-supported phylogeny, showing fourteen main lineages. Analyses of independent mitochondrial and nuclear markers supported the same main lineages, but basal relationships were not concordant. Moreover, some incongruence was found among independent mitochondrial and nuclear phylogenies. The monophyly of some poorly known genera such as Pseudophoxinus and Petroleuciscus was rejected. Representatives of both genera belong to different evolutionary lineages. Timing of cladogenetic events among the main leuciscine lineages was gained using mitochondrial and all genes data set. Conclusions Adaptations to a predatory lifestyle or miniaturization have superimposed the morphology of some species. These species have been separated into different genera, which are not supported by a phylogenetic framework. Such is the case of the genera Pseudophoxinus and Petroleuciscus, which real taxonomy is not well known. The diversification of leuciscine lineages has been determined by intense vicariant events following the paleoclimatological and hydrogeological history of Mediterranean region. We propose different colonization models of Mediterranean region during the early Oligocene. Later vicariance events promoted Leuciscinae diversification during Oligocene and Miocene periods. Our data corroborate the presence of leuciscins in North Africa before the Messinian salinity crisis. Indeed, Messinian period appears as a stage of gradually Leuciscinae diversification. The rise of humidity at the beginning of the Pliocene promoted the colonization and posterior isolation of newly established freshwater populations. Finally, Pleistocene glaciations determined the current European distribution of some leuciscine species.

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Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish.

Milan Gelnar, Andrea Šimková, Olivier Verneau … (2006)

Patterns and likely processes connected with evolution of host specificity in congeneric monogeneans parasitizing fish species of the Cyprinidae were investigated. A total of 51 Dactylogyrus species was included. We investigated (1) the link between host specificity and parasite phylogeny; (2) the morphometric correlates of host specificity, parasite body size, and variables of attachment organs important for host specificity; (3) the evolution of morphological adaptation, that is, attachment organ; (4) the determinants of host specificity following the hypothesis of specialization on more predictable resources considering maximal body size, maximal longevity, and abundance as measures of host predictability; and (5) the potential link between host specificity and parasite diversification. Host specificity, expressed as an index of host specificity including phylogenetic and taxonomic relatedness of hosts, was partially associated with parasite phylogeny, but no significant contribution of host phylogeny was found. The mapping of host specificity into the phylogenetic tree suggests that being specialist is not a derived condition for Dactylogyrus species. The different morphometric traits of the attachment apparatus seem to be selected in connection with specialization of specialist parasites and other traits favored as adaptations in generalist parasites. Parasites widespread on several host species reach higher abundance within hosts, which supports the hypothesis of ecological specialization. When separating specialists and generalists, we confirmed the hypothesis of specialization on a predictable resource; that is, specialists with larger anchors tend to live on fish species with larger body size and greater longevity, which could be also interpreted as a mechanism for optimizing morphological adaptation. We demonstrated that ecology of host species could also be recognized as an important determinant of host specificity. The mapping of morphological characters of the attachment organ onto the parasite phylogenetic tree reveals that morphological evolution of the attachment organ is connected with host specificity in the context of fish relatedness, especially at the level of host subfamilies. Finally, we did not find that host specificity leads to parasite diversification in congeneric monogeneans.

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Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: bacterial genome helps define species and evolutionary relationships in aphids.

Armelle Coeur d’acier, Yves Desdevises, Emmanuelle Jousselin (2009)

Aphids harbour an obligatory symbiont, Buchnera aphidicola, providing essential amino acids not supplied by their diet. These bacteria are transmitted vertically and phylogenic analyses suggest that they have 'cospeciated' with their hosts. We investigated this cospeciation phenomenon at a fine taxonomic level, within the aphid genus Brachycaudus. We used DNA-based methods of species delimitation in both organisms, to avoid biases in the definition of aphid and Buchnera species and to infer association patterns without the presumption of a specific interaction. Our results call into question certain 'taxonomic' species of Brachycaudus and suggest that B. aphidicola has diversified into independently evolving entities, each specific to a 'phylogenetic' Brachycaudus species. We also found that Buchnera and their hosts simultaneously diversified, in parallel. These results validate the use of Buchnera DNA data for inferring the evolutionary history of their host. The Buchnera genome evolves rapidly, making it the perfect tool for resolving ambiguities in aphid taxonomy. This study also highlights the usefulness of species delimitation methods in cospeciation studies involving species difficult to conceptualize--as is the case for bacteria--and in cases in which the taxonomy of the interacting organisms has not been determined independently and species definition depends on host association.

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Author and article information

Contributors

Michal Benovics: benovics@mail.muni.cz

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 29 August 2018

Publication date PMC-release: 29 August 2018

Publication date Collection: 2018

Volume: 8

Electronic Location Identifier: 13006

Affiliations

[1 ]ISNI 0000 0001 2194 0956, GRID grid.10267.32, Department of Botany and Zoology, Faculty of Science, , Masaryk University, ; Kotlářská 2, 61137 Brno, Czech Republic

[2 ]ISNI 0000 0001 2112 9282, GRID grid.4444.0, Sorbonne Universités, UPMC Univ Paris 06, CNRS, Biologie Intégrative des Organismes Marins (BIOM), Observatoire Océanologique de Banyuls/Mer, ; F-66650 Banyuls/Mer, France

[3 ]ISNI 0000 0004 1937 116X, GRID grid.4491.8, Department of Ecology, Faculty of Science, , Charles University in Prague, ; Viničná 7, 128 44 Prague, Czech Republic

[4 ]ISNI 0000 0001 2243 1723, GRID grid.425401.6, National Museum, ; Václavské Náměstí 68, 115 79 Prague, Czech Republic

Article

Publisher ID: 31382

DOI: 10.1038/s41598-018-31382-w

PMC ID: 6115452

PubMed ID: 30158640

SO-VID: e864a08e-13af-4389-bb03-cbff0ddbb62b

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 23 February 2018

Date accepted : 17 August 2018

Funding

Funded by: FundRef https://doi.org/10.13039/501100001824, Grantov&#x00E1; Agentura &#x010C;esk&#x00E9; Republiky (Grant Agency of the Czech Republic);

Award ID: 15-19382S

Award Recipient : Michal Benovics

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The phylogenetic relationships and species richness of host-specific Dactylogyrus parasites shaped by the biogeography of Balkan cyprinids

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Microbiota and Host

Most cited references 67

Phylogenetic relationships and biogeographical patterns in Circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data

Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish.

Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: bacterial genome helps define species and evolutionary relationships in aphids.

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Cited by 13

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