Exploring mechanisms that shape Siphonaptera composition and distribution patterns on small mammals across South Africa

Van der Mescht, Luther (2015-12)

Thesis (PhD)--Stellenbosch University, 2015.

Thesis

ENGLISH ABSTRACT: Fleas (Siphonaptera) are obligate ectoparasites of mammals and birds. Due to their economic importance as disease vectors, most contemporary studies on macroparasites now also consider the spatial variation of parasite communities and the underlying mechanisms involved in shaping current distribution patterns. Fleas differ in life history traits, such as the level of host specificity and microhabitat preferences, which can result in differential evolutionary responses to similar abiotic events. The main objectives of this study are to investigate: (1) the influence of vicariance and host association on the genetic structure of two generalist flea species, Listropsylla agrippinae, and Chiastopsylla rossi. The taxa differ in the time spent on the host (fur vs. nest) and the level of host specificity; (2) the taxonomy of Dinopsyllus ellobius to determine whether more than one species exist and if so to then elucidate the mechanisms of speciation; and (3) the influence of flea life history on species distribution model performance and see if the relative importance of predictor variables differ between species with different life histories. A total of 1423 small mammals were brushed to collect 2906 flea individuals originating from 31 geographically distinct localities throughout South Africa (SA). Phylogeographic structure of L. agrippinae and C. rossi were determined by making use of 315 mitochondrial COII (mtDNA) and 174 nuclear EF1-α (nDNA) sequences. The more host specific fur flea, L. agrippinae, displayed pronounced spatial phylogeographic structure, based on mtDNA, which was congruent with host vicariance in the region. In contrast, the more generalist nest flea, C. rossi, showed a higher level of inter-populational divergence, based on mtDNA and nDNA, and this may be attributed to comparatively higher restrictions to dispersal when compared to the more specific fur flea. In an attempt to resolve the taxonomy of D. ellobius, 151 mtDNA and 68 nDNA alleles were generated from individuals meeting the morphological description of D. ellobius. Two distinct D. ellobius lineages that corresponded to previously described species (D. ellobius and D. abaris) were recorded. The results indicate that the two species indeed differ morphologically and based on the distribution of the two species it was concluded that the diversification could be a result of climate driven vicariance and subsequent ecological segregation according to habitat use. Locality records from Segerman (1995) were digitized and used as background data in species distribution modelling. Sufficient information was obtained for 21 flea species. A total of 68 climatic and landscape feature predictor variables were obtained and through a process of elimination, 19 variables were ultimately used. Model performance was good to excellent on average and the contribution of climate and landscape feature variables differed between fleas with different life histories. Historical and contemporary climate has the most prominent effect on flea distribution at the regional scale, but the level of host association influences the phylogeographic pattern of fleas. This study provides the first evidence of congruent phylogeographic patterns between a generalist temporary parasite and its hosts. Our findings provide further support for the notion that more than one species exist within the D. ellobius complex and that speciation is a result of complex interactions. The study also provides novel data on the role of environmental variables in shaping the geographic distribution of flea species with different life histories. With the anticipated rise in flea-borne diseases worldwide, due to changes in vector distribution, the study further emphasize the need for studying the mechanisms involved in shaping flea distribution patterns.

AFRIKAANSE OPSOMMING: Vlooie (Siphonaptera) is verpligte ektoparasiete van soogdiere en voëls. As gevolg van hul ekonomiese belangrikheid as vektore van oordraagbare siektes, neem meeste kontemporêre studies oor makroparasiete nou die ruimtelike variasie (vikariansie) van parasiet gemeenskappe en die onderliggende meganismes betrokke by die vorming van die huidige verspreiding patrone in ag. Vlooie verskil in lewensgeskiedenis eienskappe, soos die graad van gasheer spesifisiteit en mikrohabitat voorkeur, wat kan lei tot differensiële evolusionêre patrone tot soortgelyke abiotiese gebeure. Die belangrikste doelwitte van hierdie studie is om ondersoek in te stel na: (1) die invloed van vikariansie en gasheer assosiasie op die genetiese struktuur van twee algemene vlooi spesies, Listropsylla agrippinae en Chiastopsylla rossi. Die taxa verskil in die hoeveelheid tyd wat gespandeer word op die gasheer (pels vs. nes) en die graad van gasheer spesifisiteit; (2) die taksonomie van Dinopsyllus ellobius om te bepaal of daar meer as een spesie bestaan, en indien wel, die meganismes van spesiasie voortbring; en (3) die invloed van vlooi lewensgeskiedenis op die prestasie van die spesies verspreidings model en kyk of die relatiewe belangrikheid van omgewingsvoorspellers verskil tussen spesies met verskillende lewensgeskiedenisse. 'n Totaal van 1423 klein soogdiere is geborsel om 2906 vlooi individue afkomstig van 31 geografies verskillende plekke in Suid-Afrika in te samel. Filogeografiese struktuur van L. agrippinae en C. rossi is bepaal deur gebruik te maak van 315 mitochondriale COII (mtDNA) en 174 kern EF1-α (nDNA) volgorde bepalings. Die meer gasheer spesifieke pels vlooi, L. agrippinae, het ruimtelike filogeografiese struktuur aangetoon, gebaseer op mtDNA, wat ooreenstem met gasheer vikariansie in die streek. In teenstelling hiermee het die minder gasheer spesifieke nes vlooi, C. rossi, 'n hoër vlak van inter-populasie divergensie getoon, gebaseer op mtDNA en nDNA, wat toegeskryf kan word aan relatief hoër beperkings op verspreiding teenoor die meer gasheer spesifieke pels vlooi. In 'n poging om die taksonomie van D. ellobius op te los is 151 mtDNA en 68 nDNA allele gegenereer uit individue wat voldoen aan die morfologiese beskrywing van D. ellobius. Twee afsonderlike D. ellobius afstammelinge wat ooreengestem het met voorheen beskryfde spesies (D. ellobius en D. abaris) is aangeteken. Die resultate dui daarop dat die twee spesies inderdaad morfologies verskil en gebaseer op die verspreiding van die twee spesies is daar tot die gevolgtrekking gekom dat die diversifikasie moontlik toegeskryf kan word aan klimaat gedryfde vikariansie en daaropvolgende ekologiese segregasie volgens habitat gebruik. Geografiese verspreidings rekords van Segerman (1995) was gedigitaliseerd en gebruik as agtergrond data in die spesie verspreidings modelle. 'n Totaal van 68 klimaat en landskap kenmerk voorspeller veranderlikes is verkry, en deur 'n proses van eliminasie, is 19 veranderlikes gebruik. Model prestasie was oor die algemeen goed tot uitstekend en die bydrae van klimaat en landskaps veranderlikes het verskil tussen vlooie met verskille in lewensgeskiedenis. Historiese en kontemporêre klimaat het die mees prominente effek op vlooi verspreiding by die plaaslike skaal, maar die vlak van die gasheer assosiasie beïnvloed die filogeografiese patroon van vlooie. Hierdie studie bied die eerste getuienis van ooreenstemmende filogeografiese patrone tussen 'n minder gasheer spesifieke, tydelike parasiet en sy gashere. Ons bevindinge bied verdere ondersteuning vir die idee dat meer as een spesie bestaan binne die D. ellobius kompleks en dat spesiasie 'n gevolg is van komplekse interaksies. Die studie bied ook nuwe data oor die bydrae van die omgewingsveranderlikes in die vorming van die geografiese verspreiding van vlooi spesies met verskillende lewensgeskiedenisse. Met die verwagte styging in vlooi-oordraagbare siektes wêreldwyd, as gevolg van veranderinge in vektor verspreiding, beklemtoon die studie verder die noodsaaklikheid vir die bestudering van die meganismes betrokke in die vorming van vlooi verspreiding patrone.

Please refer to this item in SUNScholar by using the following persistent URL: http://hdl.handle.net/10019.1/97768
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