A molecular genetic perspective on the evolution of Hyalomma ticks with emphasis on the phylogeography of H. truncatum

Sands, Arthur Francis (2016-03)

Thesis (MSC)--Stellenbosch University, 2016.

Masters

ENGLISH ABSTRACT: The tick genus Hyalomma is spread throughout the old world and species in this genus are vectors of a number of harmful pathogens. This makes them of key veterinary and medical importance, yet their systematics, and the factors giving rise to their diversity, remain largely unknown. As different species, and even different lineages, can vary in vector potential and level of acaricide resistance, it is thus of particular importance to resolve the systematics of the genus. To resolve the systematics of the genus and to obtain better insights into the mechanisms that play a role in tick evolution, the present study used both a phylogeographic and phylogenetic approach. The aims of the study were: 1) to provide a phylogeographic perspective for H. truncatum using the mtDNA COI and nDNA H3 and CRT gene regions, and 2) to create a comprehensive phylogeny for all the described extant Hyalomma species by using morphological and molecular data, derived from multiple nuclear and mitochondrial genetic markers (COI, 16S, 28S, ITS II and H3). By making use of phylogeographic networks, AMOVA analyses and Bayesian analyses, 186 H. truncatum specimens could be divided into two lineages across Africa (with a northern and southern clade). Historical demographic population analyses suggest that the two clades have different evolutionary histories, and support the notion that they have been isolated for a prolonged period time. On a regional scale, the northern clade showed higher levels of substructure with five COI phylogroups over the sampled region. The geographical positioning of these phylogroups aligns with those seen in multiple species of ungulates, primates and rodents, and it is argued that they have formed as a result of glacial cycles that caused shifts in the distribution of host species. The southern clade lacked substructure (probably due to the lack of geographic barriers to gene flow in the region). A COI sequence distance of 9.88% (SD ± 0.40%) and significant population differentiation at nuclear DNA level suggest that the two continental lineages probably represent separate species. To gain further insights into the status of H. albiparmatum and H. nitidum, and the species status of the two H. truncatum clades, a higher level systematic study was conducted on 82 specimens inclusive of all recognised Hyalomma species. Three nDNA markers (ITS II, 28S and H3), two mtDNA markers (COI and 16S) and 47 morphological characters were used to resolve relationships among Hyalomma species. Parsimony and Bayesian analyses were performed and a dated phylogeny was also constructed using available fossil data. The data suggests that the first diversification within Hyalomma began around 36.25 Mya (95% HPD 34.75-39.80 Mya) and thereafter later divergences gave rise to five groups. Since Hyalomma have limited dispersal capabilities off the host, it is likely that mechanisms responsible for speciation events are more than likely coupled to vicariance events separating multiple hosts. Certainly several faunal exchanges between zoogeographic regions such as those associated with the African-Eurasian land bridge across the Arabian plate 16-20 Mya can be correlated to speciation in Hyalomma. Furthermore sea-level oscillations of the Mediterranean Sea degradation of the Paratethys Sea, and the development of the Himalayan mountainous belt and the East African Rift Valley have been proposed as mechanisms driving speciation in a number of host such as ungulates and rodents. Although these events likely played a role in early Hyalomma evolution, substantiating the mechanisms involved in the recent divergences of many extant Hyalomma species remains difficult. The latter is mainly due to the availability of limited knowledge on the exact ranges and host associations of several taxa. Nevertheless, the results documented in this thesis propose a number of changes to the current taxonomy of the genus: 1) Ticks recognized as H. truncatum comprised of two distinct species. Following conventional zoological nomenclature, we propose the southern clade of H. truncatum to likely represent a novel species (H. species nova). 2) Hyalomma marginatum and H. turanicum should be regarded as synonyms. 3) Hyalomma nitidum should be synonymized with the H. truncatum clade found in north Africa, while H. albiparmatum should remain a distinct species entity.

AFRIKAANSE OPSOMMING: Die bosluis genus Hyalomma se verspreiding strek oor die hele Ou Wêreld en spesies in die genus is draers van 'n aantal skadelike patogene. Dus is hulle van veeartsenykundige en mediese belang, maar hul sistematiek asook die faktore wat aanleiding gee tot hul diversiteit bly grootliks onbekend. Aangesien verskillende spesies, en selfs verskillende genetiese groepe binne spesies, verskillende vlakke van akarisidiese weerstand en patogeen potensiaal kan hê, is dit van besondere belang om die sistematiek van die genus te bepaal. Ten einde die sistematiek van die genus te bepaal en beter insig tot die maganismes betrokke by bosluis evolusie te bekom, het die huidige studie beide ‘n filogeografiese en filogenetiese benadering gevolg. Die doelwitte van die studie was as volg: 1) om ‘n filogoegrafiese perspektief vir H. truncatum te verskaf deur gebruik te maak van die mitokondriale (mtDNA) COI en nukluêre (nDNA) H3 en CRT geen merkers, en 2) om ‘n omvattende filogenie vir alle beskryfde ekstante Hyalomma spesies daar te stel deur beide morfologiese en molekulêre data, afkomstig van verskeie nukluêre en mitokondriale genetiese merkers (COI, 16S, 28S, ITS II en H3), te gebruik. Filogoegrafiese netwerke, AMOVA ontledings, en die bou van 'n Bayesiaanse topologie, het aangedui dat 186 H. truncatum monsters, onderverdeel kan word in twee genetiese groepe binne Afrika (met ‘n noordelike en suidelike klade). Historiese demografiese bevolkings-resultate dui daarop dat die twee groepe se evolusionêre geskiedenis van mekaar verskil, wat moontlik ondersteunig verleen aan die idee dat hulle vir 'n lang tyd reeds van mekaar geïsoleer is. Op die streek vlak is ‘n hoër graad van substruktuur, met onderverdeling tot vyf filo-groepe regoor die studie gebied, binne die noordelike klade gevind. Die geografiese plasing van hierdie filogroepe stem ooreen met dié wat reeds in verskeie ander spesies van hoefdiere, primate en knaagdiere beskryf is. Dit word aangevoer dat hierdie patrone weens gletser siklusse, wat verskuiwings van gasheer spesies se verspreidings versoorsaak het, tot stand gebring is. Daarteen het die suidelike klade geen substruktuur getoon nie (waarskynlik as gevolg van die gebrek aan geografiese hindernisse tot geenvloei binne die verspreiding). ‘n COI volgorde afstand van 9,88% (SD% ± 0,40) gekoppel met beduidende populasie differensiasie op die nukluêre DNS vlak, stel voor dat die twee kontinentale genetiese groepe heel moontlik as twee aparte spesies beskou kan word. Om verder insigte rondom die status van H. albiparmatum en H. nitidum, asook die spesie status van die twee genetiese groepe binne H. truncatum, te bekom, is 'n hoër-vlak sistematieke studie met 82 monsters van alle erkende Hyalomma spesies onderneem. Drie nDNA merkers (ITS II, 28S en H3), twee mtDNA merkers (COI en 16S) en 47 morfologiese karakters is gebruik om verwantskappe tussen Hyalomma spesies op te los. Parsimoniese en Bayesiaanse ontledings is uitgevoer en 'n gedateerde filogenie, wat gebruik maak van beskikbare fossiel data, is ook gebou. Die data dui daarop dat die eerste diversifikasie binne Hyalomma rondom 36.25 Mjg (miljoen jaar gelede) begin het (95% HPD 34.75-39.80 Mjg) en daarna met gereelde tussenposes plaasgevind het, en sodoende gelei het tot die ontstaan van vyf groepe. Aangesien Hyalomma se verspreidings-vermoë af van die gasheer beperk is, is dit waarskynlik dat meganismes verantwoordelik vir spesiasie gekoppel was aan vikariansie gebeurtenisse binne ‘n verskeindenheid van gashere. Verskeie fauna-uitwisselings tussen zoo-grafieses streke, soos dié wat verband hou met die Afrika-Eurasiese landbrug oor die Arabiese plaat 16-20 Mjg, korreleer met spesiasie binne Hyalomma. Verder is die ossillasie van watervlakke in Parathetys see asook die ontwikkeling van die Himalaja-gordel en Oos-Afrika Rift Vallei voorgestel as meganismes wat spesiasie binne verskeie gashere, soos hoefdiere en knaagdiere, gedryf het. Alhoewel hierdie gebeurtenisse waarskynlik ‘n rol gespeel het by vroeë Hyalloma evolusie, is dit steeds moeilik om die meganismes betrokke by die onlangse divergensies van verskeie Hyalomma spesies te staaf, weens beperkte kennis rondom die presiese omvang van verspreidings en gasheer assosiasies van verskeie taksa. Ongeag hiervan, dui die resultate van hierdie tesis op 'n aantal voorgestelde veranderinge aan die huidige taksonomie van die genus: 1) Die tans erkende H. truncatum bestaan uit twee afsonderlike spesies. Op grond van konvensionele dierkundige nomenklatuur stel ons voor dat die suidelike klade van H. truncatum waarskynlik 'n nuwe spesie is (H. spesies nova). 2) Hyalomma marginatum en H. turanicum moet beskou word as sinonieme. 3) Hyalomma nitidum moet verklaar word as ‘n sinoniem tot die H. truncatum klade wat binne noord-Afrika voorkom, terwyl H. albiparmatum 'n afsonderlike spesie entiteit behoort te bly.

Please refer to this item in SUNScholar by using the following persistent URL: http://hdl.handle.net/10019.1/98279
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