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Evidence of cryptic species in the genus Tinaminyssus (Acari: Rhinonyssidae) based on morphometrical and molecular data

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  • Pavlov First Saint Petersburg State Medical University; Zoological Institute of Russian Academy of Sciences
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Abstract and Figures

The study of cryptic species allows to describe and to understand biodiversity, and the evolutionary processes shaping it. Mites of the family Rhinonyssidae are permanent parasites of the nasal cavities of birds, currently including about 500 described species and 12 genera. Here, we tested the hypothesis that mites from five populations of the genus Tinaminyssus—three isolated from European turtle doves (Streptopelia turtur), and two from Eurasian collared doves (Streptopelia decaocto; Aves: Columbiformes)—are, in fact, two cryptic species inhabiting different hosts. First, we performed a morphometrical study on 16 traits. Then, we used the ITS1-5.8S rDNA-ITS2 nuclear region (ITS region), and a fragment of the mitochondrial cytochrome c-oxidase 1 (COI) to carry out phylogenetic and species delimitation analyses on Tinaminyssus species. Morphological analyses revealed a lack of biometric differentiation among Tinaminyssus populations from the two host species. However, molecular analyses indicated a high degree of genetic differentiation between populations of Tinaminyssus sp. from S. turtur and S. decaocto. Overall, results show that they can be considered as different cryptic species, suggesting a case of evolutionary stasis, likely because of the anatomical similarity between closely-related bird host species.
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Exp Appl Acarol (2018) 75:355–368
https://doi.org/10.1007/s10493-018-0271-x
1 3
Evidence ofcryptic species inthegenus Tinaminyssus
(Acari: Rhinonyssidae) based onmorphometrical
andmolecular data
ManueldeRojas1 · JorgeDoña2,3 · RogerJovani2 · IvanDimov4·
AntonioZurita1 · RocíoCallejón1 · MaríaRodríguez‑Plá1
Received: 3 August 2017 / Accepted: 24 May 2018 / Published online: 6 June 2018
© Springer International Publishing AG, part of Springer Nature 2018
Abstract The study of cryptic species allows to describe and to understand biodiversity,
and the evolutionary processes shaping it. Mites of the family Rhinonyssidae are perma-
nent parasites of the nasal cavities of birds, currently including about 500 described spe-
cies and 12 genera. Here, we tested the hypothesis that mites from five populations of the
genus Tinaminyssus—three isolated from European turtle doves (Streptopelia turtur), and
two from Eurasian collared doves (Streptopelia decaocto; Aves: Columbiformes)—are, in
fact, two cryptic species inhabiting different hosts. First, we performed a morphometrical
study on 16 traits. Then, we used the ITS1-5.8S rDNA-ITS2 nuclear region (ITS region),
and a fragment of the mitochondrial cytochrome c-oxidase 1 (COI) to carry out phyloge-
netic and species delimitation analyses on Tinaminyssus species. Morphological analyses
revealed a lack of biometric differentiation among Tinaminyssus populations from the two
host species. However, molecular analyses indicated a high degree of genetic differenti-
ation between populations of Tinaminyssus sp. from S. turtur and S. decaocto. Overall,
results show that they can be considered as different cryptic species, suggesting a case of
evolutionary stasis, likely because of the anatomical similarity between closely-related bird
host species.
Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s1049
3-018-0271-x) contains supplementary material, which is available to authorized users.
* Manuel de Rojas
derojas@us.es
1 Department ofMicrobiology andParasitology, Faculty ofPharmacy, University ofSevilla,
Profesor García González 2, 41012Seville, Spain
2 Department ofEvolutionary Ecology, Estación Biológica de Doñana (EBD-CSIC), Avda. Americo
Vespucio 26, 41092Seville, Spain
3 Illinois Natural History Survey, Prairie Research Institute, University ofIllinois atUrbana-
Champaign, 1816S. Oak St., Champaign, IL61820, USA
4 Department ofHuman Anatomy, State Pediatric Medical University, Litovskaya St. 2,
St.Petersburg, Russia194100
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... For this purpose, our dataset was aligned with other ITS1-5.8S-ITS2 sequences that were obtained previously [25,26] The resulting phylogenetic tree was analyzed according to the current taxonomy of the family Rhinonyssidae. Our data addressed some taxonomic questions, such as the status of the taxa included in species complexes that comprise very closely related species, and the usefulness of cheliceral morphology for identifying genera. ...
... Morphometrical measurements of the dorsal and ventral sides of Tinaminyssus spp., Ptilonyssus spp., Rhinonyssus spp., and Sternostoma spp. were made, namely, the length of the body (including palps) (LB), the width of the idiosoma (WI), the length of the podosomal shield (LPS), the width of the podosomal shield (WPS), the length of the opisthosomal shield (LOS), the width of the opisthosomal shield (WOS), the length of the anal shield (LAS), the width of the anal shield (WAS), the length of the ventral view of the gnathosoma (including palps) (LG), and the width of the gnathosoma (WG) [26]. ...
... They are gathered together (100/92), and the genetic distance between them (0.11) is similar to that between T. streptopeliae and T. melloi (0.14), which are different species. This agrees with de Rojas et al. [26], who considered the former species to be a cryptic species. ...
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Members of the family Rhinonyssidae are tiny hematophagous endoparasitic mites that inhabit the nasal cavities of birds and can cause trauma to their hosts. Traditionally, identifying species in this group has relied on observing their morphometrical characteristics. Nevertheless, determining species within this particular group has become more challenging due to the rising number of newly discovered species. Moreover, the morphometrical traits vary depending on the specific genus or group of species being studied. In this study, the complete internal transcribed spacer ITS1, 5.8S rDNA, and ITS2 regions of the ribosomal DNA from eighteen species of rhinonyssid mites belonging to four genera were sequenced to assess the utility of this genomic region in resolving taxonomic questions in this group and to estimate the phylogenetic relationships among the species. Mites were collected by dissecting the nasal cavities of birds under a stereomicroscope. Specimens used for morphometrical analyses were cleared in 85% lactic acid for 1–48 h and mounted in Hoyer’s medium. Other specimens were preserved at −20 °C for molecular studies. From the data obtained in this study, it can be concluded that a thorough review and an accurate morphometrical identification and determination of the discriminatory traits are needed in this group of mites. Moreover, although the ITS1–5.8S–ITS2 fragment solves different taxonomic and phylogenetic problems at the species level, it would be necessary to test new molecular markers, or even a combination of nuclear and mitochondrial markers or different domains of the nuclear 28S rDNA, to discover a reliable taxonomic situation for rhinonyssids.
... Most species live in the nasal cavity on the vascularised epithelial tissue; nevertheless, some species occupy the lungs, tracheal tissues and body cavity of their hosts (Lindquist et al. 2009;). Rhinonyssids can not only cause damage to their hosts in a direct way (Rhinonyssidosis avium disease) (Dimov 2011), but could also be reservoirs or vectors of other infections like West Nile fever, Q fever, avian influenza and Lyme disease, as have been shown in mites from the family Dermanyssidae (Reeves et al. 2006). Despite their ecological relevance, most aspects of the basic biology, ecology and evolution of these mites are still poorly understood. ...
... Confidence intervals of prevalence (95%) are provided between parentheses. Butenko 1984;Cerny 1970;Crossley 1951;Domrow 1965;Domrow 1966a;Domrow 1966b;Fain 1956;Fain 1957;Fain 1958;Fain 1962b;Fain et al. 1974;Pence 1975;Sixl 1971;Wilson 1964 Butenko 1965;Fain 1956;Fain 1957;Fain 1959;Fain 1962a;Fain 1963;Fain and Aikten 1967;Fain et al. 1974;Furman 1957;Pence 1972c;Shumilo and Lunkashu 1970;Sixl 1971;Spicer 1984;Spicer 1987 Butenko 1965;Fain 1956;Fain 1957;Fain 1959;Fain 1962a;Fain 1963;Fain and Aikten 1967;Fain et al. 1974;Furman 1957;Pence 1972c;Shumilo and Lunkashu 1970;Sixl 1971;Spicer 1984;Spicer 1987 Butenko 1965;Fain 1956;Fain 1957;Fain 1959;Fain 1962a;Fain 1963;Fain and Aikten 1967;Fain et al. 1974;Furman 1957;Pence 1972c;Shumilo and Lunkashu 1970;Sixl 1971;Spicer 1984;Spicer 1987 Butenko 1965;Fain 1956;Fain 1957;Fain 1959;Fain 1962a;Fain 1963;Fain and Aikten 1967;Fain et al. 1974;Furman 1957;Pence 1972c;Shumilo and Lunkashu 1970;Sixl 1971;Spicer 1984;Spicer 1987 Butenko 1965;Fain 1956;Fain 1957;Fain 1959;Fain 1962a;Fain 1963;Fain and Aikten 1967;Fain et al. 1974;Furman 1957;Pence 1972c;Shumilo and Lunkashu 1970;Sixl 1971;Spicer 1984;Spicer 1987 ...
... In addition, new molecular approaches (e.g. DNA metabarcoding of complex samples; Doña et al. 2019) would help to accelerate the discovery of new species along with validating the species status of previously-described rhinonyssid species, as cryptic species are known in this group (de Rojas et al. 2018). ...
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Rhinonyssid mites are permanent parasites of birds that inhabit their respiratory tract. There are around 600 species described worldwide and almost all species of birds are found to have embedded rhinonyssid mites. Despite their presumed relevance, these mites are largely unstudied due to the difficulty in sampling them and, therefore, the majority of mite-host associations and species-prevalence data are unknown. In this study, 179 mite specimens belonging to 27 species and eight genera were identified. Notably, 18 new mite-bird associations were documented for the first time, thus increasing the known host range for these mite species. In addition, mite-host associations found in this study were compared with known associations from these species of birds in the European part of Russia and in Europe. Overall, this study represents the largest survey to date carried out on rhinonyssid mites in Russia and one of the most comprehensive datasets on rhinonyssid host-range.
... Rhinonyssid mites have been reported on C. livia in the USA (Crossley, 1950;Pence, 1975), Canada (Knee & Proctor, 2010;Knee et al., 2008;Wilson, 1964), Russia (de Rojas et al., 2020) and Spain (de Rojas et al., 2018(de Rojas et al., , 2001(de Rojas et al., , 2002Úbeda et al., 2003), while Ereynetidae mites has been recorded in this host in the USA (Crossley, 1952) and Australia (Domrow, 1969). In Brazil, there is only 1 record of Tinaminyssus melloi (Castro, 1948) (Rhinonyssidae) described as a parasite in C. livia (Castro, 1948). ...
... The mite species found in the present study has wide geographic distribution since it was registered in the American continent, Russia, Spain, Australia, and Africa. Tinaminyssus columbae and T. melloi were recorded in C. livia in the USA (Crossley, 1950;Pence, 1975), Canada (Knee & Proctor, 2010;Knee et al., 2008;Wilson, 1964), Russia (de Rojas et al., 2020) and Spain (de Rojas et al., 2001(de Rojas et al., , 2002(de Rojas et al., , 2018Úbeda et al., 2003). In addition, T. melloi was found in Zenaida macroura Linnaeus, 1758 in Canada (Knee & Proctor, 2010;Knee et al., 2008). ...
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This study aims to record mites associated with the respiratory system of Columba livia Gmelin, 1789, including data of parasitological indices and of coinfections in southern Brazil. Two hundred and two specimens of C. livia were collected in the urban area in Pelotas, Rio Grande do Sul (RS) state, Brazil. Fifty-six (27.7%) birds were parasitized by Rhinonyssidae and Ereynetidae mites. Tinaminyssus columbae (Crossley, 1950) and Tinaminyssus melloi (Castro, 1948) (Rhinonyssidae) were found in nasal cavities and tracheae of the birds. Trispeleognathus striatus (Crossley, 1952) (Ereynetidae) was found in hosts’ nasal cavities. The prevalence of Rhinonyssidae mites (25.2%) was significantly higher than obtained for Ereynetidae (5.9%). Coinfections only occurred in nasal cavities of 8 (3.96%) birds. This study records for the first time T. columbae and Trispeleognathus striatus parasitizing C. livia in Brazil. In addition, mite infection indices and coinfections of Rhinonyssidae and Ereynetidae mites in this Columbidae species are recorded.
... This finding supports the selection of 28S as a suitable marker, which is consistent with previous studies that reported limited intraspecific variation in avian intranasal acari using markers such as ITS1-5.8S-ITS2 and COI [39]. ...
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... Columbiformes are parasitized by Tinaminyssus Strandtmann & Wharton, 1958 (Rhinonyssidae) and Trispeleognathus Fain, 1957 (Ereynetidae) species (Pence 1975;Mascarenhas et al. 2018). Columba livia Gmelin, 2020 was recorded as a host of Tinaminyssus columbae (Crossley, 1950) and Tinaminyssus melloi (Castro, 1948) in Brazil (Castro 1948;Porto et al. 2022), the USA (Crossley, 1950;Wilson 1964), Canada (Knee and Proctor 2010), Spain (Úbeda et al. 2003;De Rojas et al. 2018;Veiga et al. 2021), andRussia (De Rojas et al. 2020), while it also hosted Trispeleognathus striatus (Crossley, 1952) in the USA (Crossley 1952), Australia (Domrow 1969), and Brazil (Porto et al. 2022). Additionally, T. melloi was recorded in C. livia in Hungary (Rózsa 1990) and the Canary Islands (Foronda et al. 2004). ...
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... A large amount of cryptic speciation has been described for various groups of mites, including parasites and commensals of vertebrates (Dabert et al., 2001;Deunff et al., 2004;Zhao et al., 2014), plant pests (Umina et al., 2004;Navia et al., 2013;Skoracka et al., 2017), water mites (Fisher et al., 2017;Pešić et al., 2017;Blattner et al., 2019) and soil-inhabiting mites (Walter and Campbell, 2003;Schäffer et al., 2019). In addition, the phenomenon of morphological stasis has been reported for mites (Skoracka et al., 2012;de Rojas et al., 2018;Pfingstl et al., 2019), but it was formally tested only by Heethoff et al. (2007) (Pepato et al., 2018). It should be noted that the date of Linopodes origin closely synchronises with that of the J/K boundary (ca. ...
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... Indeed, some recent studies have indicated that colonisation opportunities may be underestimated for some of these symbionts with limited transmission capabilities, and clade-limited host-switching may occur frequently [25][26][27][28] . Alternatively, multi-host symbiont species from relatively host-specific symbionts could represent undiscovered cryptic species [29][30][31][32][33] . Indeed, cryptic species might be common in small-bodied symbionts inhabiting closely related hosts, because these hosts can offer a similar habitat, and therefore, there might be strong selective pressure for highly similar symbiont phenotypes 34 . ...
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The recently-developed statistical method known as the "bootstrap" can be used to place confidence intervals on phylogenies. It involves resampling points from one's own data, with replacement, to create a series of bootstrap samples of the same size as the original data. Each of these is analyzed, and the variation among the resulting estimates taken to indicate the size of the error involved in making estimates from the original data. In the case of phylogenies, it is argued that the proper method of resampling is to keep all of the original species while sampling characters with replacement, under the assumption that the characters have been independently drawn by the systematist and have evolved independently. Majority-rule consensus trees can be used to construct a phylogeny showing all of the inferred monophyletic groups that occurred in a majority of the bootstrap samples. If a group shows up 95% of the time or more, the evidence for it is taken to be statistically significant. Existing computer programs can be used to analyze different bootstrap samples by using weights on the characters, the weight of a character being how many times it was drawn in bootstrap sampling. When all characters are perfectly compatible, as envisioned by Hennig, bootstrap sampling becomes unnecessary; the bootstrap method would show significant evidence for a group if it is defined by three or more characters.
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A new species of quill mites (Syringophilidae) Syringophiloidus plocei sp. nov. parasitizing Ploceus cucullatus (St. Muller) (type host), P. aurantius (Vieillot) and P. nigerrimus (Vieillot) (Ploceidae: Passeriformes) in Gabon is described using external morphology and DNA barcode data (the mitochondrial cytochrome c oxidase subunit I sequences (COI) and D1–D3 region of the nuclear 28S rRNA gene). Females of S. plocei sp. nov. differ from S. pseudonigritae Glowska, Dragun-Damian and Dabert, 2012 by the length of setae ag3 190–230 (vs 145–160). The genetic distances (K2P) between COI haplotypes of S. plocei sp. nov. individuals (from P. cucullatus, P. nigerrimus and P. aurantius) and S. pseudonigritae ranges from 13.1–13.7%.