Habitat fragmentation, patterns of diversity and phylogeography of small mammal species in the Albertine rift

• Main Author: Kaleme, Prince K.
• Other Authors: Jansen van Vuuren, Bettine, Bowie, Rauri C. K., Bates, John M., Stelenbosch University. Faculty of Science. Dept. of Botany and Zoology.
• Format: Thesis
• Language: English
• Published: Stellenbosch : Stellenbosch University 2013
• Subjects: DNA sequence; Phylogenetic analyses; Traditional morphometrics; Geometric morphometrics; Mammals; Small mammals; Albertine rift; Botany & Zoology; Byna; Maak; Norway; Tussen; Rattus rattus
• Online Access: http://hdl.handle.net/10019.1/18110

Thesis (PhD) - Stellenbosch University, 2011. ENGLISH ABSTRACT: The Albertine Rift is characterized by a heterogeneous landscape which may, at least in part, drive the exceptional biodiversity found across all taxonomic levels. Notwithstanding the biodiversity and beauty of the region, large areas are poorly understood because of political instability with the inaccessibility of most of the region as a contributing factor. The majority of studies in the Albertine Rift have focussed on charismatic mega fauna, with other taxa receiving less attention. One of the taxonomically and numerically more abundant small mammal genera is the genus Praomys, an African endemic with a wide distribution range spanning most of west, central and east Africa. Four species are typically recognized from the Albertine Rift namely P. degraaffi, P. jacksoni, P. misonnei and P. verschureni. In this study I used a combination of DNA sequence data (mitochondrial control region, mitochondrial cytochrome b and 7th intron of the nuclear ß-fibrinogen gene) as well as morphometric data (traditional and geometric) to investigate the systematics of the Praomys taxa occurring in the Albertine Rift. To allow meaningful DNA assessments and in an attempt to identify potential drivers of diversifications, other Praomys species were also included from public sequence data bases for comparisons. The main focus was on P. jacksoni (the numerically most abundant taxon; also, up to 2005, all Praomys in the Albertine Rift were mostly collected as “jacksoni”) and P. degraaffi (an Albertine Rift endemic). A surprising finding was the presence of P. mutoni; this represents a range extension for this species into the Albertine Rift. Distinct evolutionary lineages were found in both P. jacksoni (confirmed by sequence data as well as morphometrics) as well as P. degraaffi (based only on sequence data; insufficient samples precluded a full morphometric investigation). These lineages (in both P. jacksoni as well as P. degraaffi) appear to be separated along a north – south gradient; however, further investigations should confirm this. To further investigate the genetic patterns at local scales across the Albertine Rift, as well as introgression between species as revealed by sequence data, a species-specific microsatellite library was developed for P. jacksoni. Twelve polymorphic markers were identified of which nine also amplified in P. degraaffi. Introgression was confirmed between the two focal species with almost 20% of the individuals analysed being jacksoni-degraaffi hybrids. This is perhaps not so surprising given that there is considerable overlap in their ranges (between ~ 1500 m a.s.l. to 2450 m a.s.l.) as well as the relative ages of the species (the divergence time between these two species were estimated at 3.8 Mya). The presence of distinct lineages within each of these species was confirmed by microsatellite analyses (these lineages diverged approcimately at same time at ca. 3.4 Mya). As suggested by sequence and morphometric data, these lineages had a largely north – south distribution but with considerable overlap in the central Albertine Rift in the vicinity of Lake Kivu. The phylogeographic patterns obtained for both focal species were not consistent with the physical barriers such as the rivers, lakes or mountains, nor were they exclusively associated with Pleistocene phenomena such as the change of the course of the rivers or uplift; rather, the lineages predate the Pleistocene and fall firmly in the Pliocene (>3 Mya). Biogeographically, the north - south location of lineages with a centrally - located contact zone could be a result of parapatric speciation due to habitat fragmentation or past climate change, followed by secondary contact. Barcoding using genetic information provides a useful tool to identify unknown taxa, cryptic diversity or where different life stages are difficult to identify. From an invasion biology perspective, it allows for the rapid identification of problem taxa against a known data base. By adopting such a barcoding approach (senso lato), the presence of three invasive rodents was confirmed in the Democratic Republic of the Congo (DRC); these are Rattus rattus (black rat), R. norvegicus (Norway rat) and Mus musculus domesticus (house mouse). A comparison with global data available for these species revealed two possible introduction pathways namely via the shipping port at Kinshasa/Matadi (with strong links to Europe) and via the slave trade routes in the east (strong links to the Arab world and the east). Of these three taxa, only R. rattus is currently documented from the DRC although the others have received mention in the gray literature. These findings draw attention to the lack of any official policy regarding biosecurity in the DRC, and argue for the development of strict control measures to prevent further introductions. AFRIKAANSE OPSOMMING: Die Albertine Rift word gekenmerk deur 'n heterogene landskap wat kan, ten minste gedeeltelik, die uitsonderlike biodiversiteit wat oor al die taksonomiese vlakke gevind word teweeg bring. Nieteenstaande die biodiversiteit en die skoonheid van die streek, is groot gebiede onbekend as gevolg van politieke onstabiliteit met die ontoeganklikheid van meeste van die streek as 'n bydraende faktor. Die meerderheid van studies in die Albertine Rift het gefokus op die charismatiese mega fauna, met ander taxa wat minder aandag ontvang. Een van die taksonomies en numeries meer volop klein soogdier genera is die genus Praomys, 'n Afrika endemiese groep met 'n wye verspreiding wat strek oor die grootste deel van van wes-, sentraal en oos-Afrika. Vier spesies word tipies erken van die Albertine Rift naamlik P. degraaffi, P. jacksoni, P. misonnei en P. verschureni. In hierdie studie het ek 'n kombinasie van DNA volgorde data (mitochondriale beheer streek, mitochondriale sitochroom b en 7de intron van die kern ß-fibrinogeen geen) sowel as morfometriese data (tradisioneel en meetkundig) gebruik om die sistematiek van die Praomys taxa te ondersoek. Om betekenisvolle DNA aanslae toe te laat en in 'n poging om potensiële aandrywers van diversiteit te identifiseer, is ander Praomys spesies van openbare volgorde data basisse vir vergelykings ingesluit. Die hooffokus is op P. jacksoni (die numeries volopste takson, ook, tot en met 2005 is alle Praomys in die Albertine Rift meestal as "jacksoni" versamel) en P. degraaffi ('n Albertine Rift endemiese spesie). 'n Verrassende bevinding was die teenwoordigheid van P. mutoni, dit verteenwoordig' n verspreidingsuitbreiding vir hierdie spesie in die Albertine Rift. Bepaalde evolusionêre ontwikkelingslyne was in beide P. jacksoni (bevestig deur die volgorde data sowel as morfometrie) sowel as P. degraaffi (wat slegs gebaseer is op die volgorde data, onvoldoende monsters verhinder 'n volledige morfometriese ondersoek). Hierdie lyne (in beide P. jacksoni sowel as P. degraaffi) word geskei langs 'n noord - suid gradiënt, maar verdere ondersoeke moet dit bevestig. Om die genetiese patrone op plaaslike skaal oor die Albertina Rift verder te ondersoek, sowel as introgressie tussen spesies soos geopenbaar deur die volgorde data, is 'n spesie-spesifieke mikrosatelliet biblioteek ontwikkel vir P. jacksoni. Twaalf polimorfiese merkers is geïdentifiseer waarvan nege ook amplifiseer in P. degraaffi. Introgressie is bevestig tussen die twee brandpunt spesies met byna 20% van die individue wat ontleed is as jacksoni-degraaffi basters. Dit is miskien nie so verbasend gegee dat daar aansienlike oorvleueling is in hul gebiede (tussen ~ 1500 m bo seespieel tot 2450 m bo seespieel), sowel as die relatiewe ouderdomme van die spesies (die divergensie tussen hierdie twee spesies is geskat op 3,8 Mya). Die teenwoordigheid van verskillende lyne in elk van hierdie spesies is bevestig deur mikrosatelliet ontleding (hierdie lyne het gedivergeer ongeveer 3,4 Mya). Soos voorgestel deur die DNA volgorde en morfometriese data, het hierdie lyne 'n grootliks noorde – suid verspreiding, maar met 'n aansienlike oorvleueling in die sentrale Albertine Rift in die omgewing van die Kivumeer. Die filogeografiese patrone wat vir beide die brandpunt spesies gevind is nie in ooreenstemming met die fisiese struikelblokke soos die riviere, mere of berge nie, en hou ook nie uitsluitlik verband met die Pleistoseen verskynsels soos die verandering van die loop van die riviere nie; die afstammelinge is eerder veel ouer as die Pleistoseen en val binne die Plioseen (> 3 Mya). Biogeografies, die noorde – suid plasing van die lyne met 'n sentraal geleë kontak sone kan die gevolg wees van parapatriese spesiasie te danke aan habitatfragmentasie as gevolg van verandering in die klimaat, gevolg deur 'n sekondêre kontak. Strepieskodering met behulp van genetiese inligting verskaf 'n nuttige instrument om onbekend taxa, kriptiese diversiteit of waar verskillende lewensfases moeilik is om te identifiseer, te identifiseer. Vanuit 'n indringerbiologie perspektief, maak hierdie benadering dit moontlik om vinnige identifikasies van die probleem taksa teen' n bekende data basis te bekom. Deur gebruik te maak van so 'n strepieskoderingsbenadering (senso lato), is die teenwoordigheid van drie indringende knaagdiere bevestig in die Demokratiese Republiek van die Kongo (DRK), naamlik Rattus rattus (swart rot), R. norvegicus (Noorweë rot) en Mus musculus domesticus (huis muis). 'n Vergelyking met die globale data wat beskikbaar is vir hierdie spesies het aan die lig gebring dat twee moontlike betree-roetes bestaan, naamlik via die skeepshawe by Kinshasa / Matadi (met sterk skakels na Europa), en via die slawehandel roetes in die ooste (sterk skakels na die Arabiese wêreld en die ooste) . Van hierdie drie taxa, is tans slegs R. rattus van die Demokratiese Republiek van die Kongo gedokumenteer, hoewel die ander melding ontvang in die grys literatuur. Hierdie bevindinge vestig die aandag op die gebrek aan enige amptelike beleid ten opsigte van biosekuriteit in die Demokratiese Republiek van die Kongo, en argumenteer vir die ontwikkeling van streng beheermaatreëls om verdere indringerspesies te voorkom.