FISA Bulletin (2000): 57-59

Lake Victoria Region: A natural experiment in ‘adaptive ecology’ and ‘speciation mechanisms’

Paul A. Fuerst1, Wilson W. Mwanja1 and Les Kaufman2

1 Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, Ohio 43210 USA and 2 Boston University Marine Program, Boston University, 5 Cummington St., Boston, MA 02215 , USA

Lake Victoria Region are a variety of satellite lakes, from crater lakes of western Uganda around Lakes The Lake Victoria Region (LVR) has Edward and George, swamp lakes of the long been considered a unique Kyoga basin, rift valley lakes of Kenya and zoogeographical area. Among the Tanzania, and small lake systems, such as characteristics which set it apart from other those of Nabugabo, the Koki lakes and the localities is the concentration of different lakes of the Yala system in Lake Victoria freshwater lakes within the region that each Basin. contain a repeated set of similar fish faunal groups. Evolution appears to have repeated LVR as a natural experiment itself numerous times in the LVR- some of these repetitive patterns are attributable to The differences in geology, hydrology evolutionary parallelism, while others are and limnology of different lakes of the LVR probably the result of seemingly improbable present contrasting conditions that offer but nonetheless real dispersal events among different challenges and opportunities for lake basins. It is thought that historically the scientific exploration and inquiries into fish LVR was once occupied by a more expansive faunal evolution and trends in the historical lake, with adjoining east-west running rivers. limnology of the region. Most of the lakes in This historical system broke up following the the LVR are of recent origin and are tectonic earth movements and volcanic characterized by a history of dramatic activity that characterized the early history of changes, brought about most importantly by the LVR to form the present lakes. The volcanism and/or long spells of complete LVR is now comprised of five large lakes, drying up. The largest of the lakes in the Victoria, Kyoga, Edward, George and Kivu, region, Lake Victoria, is known to have been each containing similar species groups that formed about 750,000 years ago and likely share a common origin. The lakes, geological evidence indicates that it has gone though zoogeographically similar, are through at least one, and probably several geologically, hydrologically and limnologically long cycles of completely drying up and then different from each other. Further, each of refilling. The last time of drying for Lake the large lakes in the region is associated with Victoria is thought to have occurred as surrounding minor water bodies, from a few recently as 14,000 years ago, and lasted for an to several small lakes. We commonly refer estimated 2000 years. Lake Edward is to these small lakes around large lakes as believed to have been a more expansive lake "satellite lakes" of the larger systems. There than it is presently, one that possibly stretched as far east as the shores of the adaptive radiation of the haplochromine current Lake Victoria. This history makes it cichlids into the numerous ecological habitats a possible source of progenitor fish species presented by various water bodies in the which reinvaded Lake Victoria after the last LVR, while maintaining their basic body dry spell. With volcanism, the ancient Lake plan, allows investigators to study Edward is believed to have receded and morphogenesis along phyletic lineages, and finally broken up into Lakes George, Kivu, investigate how organisms adjust the current Edward, and several satellite morphologically to changing habitat over very lakes. The history of Lake Kyoga is quite short evolutionary time scales. The different. Lake Kyoga has a mean depth of conditions in the LVR also present scientists only three meters and is a massive swampy with possibilities to correlate the limnological area thought to have been turned into a lake and geological history of the region with the when the outflow connecting Lake Victoria to history inferred from relationships derived the nilotic water system filled a shallow from the phylogeny among species of the trough on the course of River Nile to the different groups and or water bodies. north. This variety of lake geologies and lake Human influence on the Lake Victoria histories presents a scientific challenge in Region – a few ‘pleasantries’ out of an understanding the relationships among the ecological disaster water bodies and among their associated floral and faunal content. The challenge is The introduction of Nile perch and increased by the apparent similarity in fish non indigenous tilapiine fishes into the LVR species composition among lakes of the left little refuge for the native fish species, LVR. One of the most intriguing facts about especially in the big lakes. This happened at the diversity of the fish fauna, though shared a time of heightened fishing pressure, with other African Great Lakes regions, is the contributing to the collapse of the native enormous adaptive radiation of cichlid fish commercial species. The native commercial species in all the LVR lakes and the high fishes included primarily the only two native level of localized endemism associated with tilapiine species and large native predatory each of the lakes, again especially among the fish species in Lakes Kyoga and Victoria. cichlid species. It is astonishing that The collapse of the native fishery also estimates suggest that, for Lake Victoria overlapped a time of limnological changes in alone, nearly 600 species have evolved in the lake, from a predominantly diatomous only the 12,000 years which have elapsed ecosystem to one which is now blue-green since its last dry spell. algal (cyanobacterial) dominated. It could be The short evolutionary history of the argued that supplanting a native tilapia fishery fishes in the LVR presents an opportunity by a fishery based on Nile perch and Nile rarely found in other natural faunal systems tilapia has been good for the economics of anywhere else in the world. In the case of the the fishery, but the introduction of these LVR cichlids the opportunity exists to exotic species has been implicated as one of examine phylogenetic linkages with ancestral the primary causes of the worst vertebrate taxa that are actually still extant. In most extinction event of the 20th century, with an cases evolutionary relationships must be estimated 200 species of endemic cichlids reconstructed from extant species and feared completely lost. While the main lakes through fossil remains of ancestral forms in have been severely impacted by the what is often a very patchy or absent fossil introduction of exotic species, only a few of record. The enormous and repetitive the minor lakes (such as Lake Nabugabo in the Victoria Basin and Lake Nyasala in Lake extinction with every expedition made to the Kyoga Basin) have experienced the lakes. Unfortunately, large portions of the domination of the Nile perch and the extant cichlid fauna in the LVR remain INFLUENCE of its ‘extinction machinery’ undescribed, as was the largest portion of the on the endemics. In some of the minor extinct taxa. Continued changes in the lake lakes, such as Lake Bisina in Lake Kyoga ecosystem have put increased urgency on the Basin, the Nile perch flourished early need for studies to assess what is left in the following introduction, but has since been wild. This urgency exists even if there is no knocked back by selective fishing mortality. reprieve for many of the most endangered High fishing pressure and explosion of the species. We must at least try to tap the water hyacinth has also brought down the invaluable evolutionary information numbers of Nile perch in some areas of the contained in species that may be going extinct large lakes, making the waters where the Nile at a rate greater than we can currently study perch has collapsed a haven for the them. Some solace can be taken that resurgence of many original native cichlid knowledge about some of the rarer forms species. Such situations now provide us with may not yet be lost. Our exploratory surveys natural experiments on the mechanisms of so far have revealed that significant portions cichlid speciation and/or other factors that of the cichlid fauna previously considered have been thought to have led to the extinct in the large lakes may be still surviving resurgence of fish species in LVR as a whole. in several of the satellite lakes. Some of the Together with new data on the evolutionary satellite lakes, such as the Nabugabo lakes on history of the species of the LVR, on the northwestern side of Lake Victoria still information about the changing limnology, have small number of species found nowhere and on new knowledge concerning the else. Other satellite lakes, such as the Kyoga hydrological history of the region we may well lakes in central Uganda, have a wide variety begin to clarify some of the contentious of species which include both known species issues pertaining to evolutionary theories and and several undescribed species that seem to how new species are derived from existing be sister species to some now extinct from forms. The numerous satellite lakes the larger lakes. For example, we have surrounding the large lakes, the vast number discovered the scale-eating haplochromines of species, human influence, and the recent of the genus Allochromis, thought endemic history of the LVR provide us with great to Lake Victoria, alive and well, though opportunity and challenge to scientifically extremely uncommon, in the Kyoga lakes. unravel the confusing picture presented to us Although studies during the 1980's by nature. and early 1990's revealed no marked genetic differences between various Lake Victoria Species extinction – exactly how much haplochromine species, newly developed have we lost? types of molecular markers (microsatellite DNA markers), produced specifically for Despite its young age, Lake Victoria LVR haplochromine cichlid species in our is estimated to have contained over 500 laboratory, can differentiate populations and species of cichlids prior to changes in the species even at a very fine scale. We are lake caused by human activity that have taken currently using these methods to investigate place during this century. It is estimated that several phylogenetic and macroevolutionary these changes resulted in the extinction of questions in the haplochromine species. It is nearly two hundred species, and with more especially important to our understanding of species found to be at a great risk of the evolutionary and hydrological processes that have shaped the LVR system for us to century. determine whether the fish species of these The bounty of cichlid fishes in these small water bodies are of recent origin or minor lakes was first considered by reflect longer historical changes in LVR. Greenwood in several of his papers Efforts to conserve the aquatic biodiversity of (Greenwood, 1981). Among the lakes on the region hinge largely on our knowledge which Greenwood worked were the about the species and the relationships Nabugabo lakes west of Lake Victoria. He among extant evolutionary and ecological found these minor lakes to be not as speciose groups. Molecular tools have a clear as Lake Victoria but containing sister taxa to advantage in such studies because those in the larger lakes. Greenwood information about historical relationships and concluded that minor lakes can act as nursery evolutionary linkages among species, extant beds that multiply species which later move and extinct, is directly embedded in the into the larger systems. Our recent discovery molecules (DNA and enzymes) targeted by in satellite lakes in the LVR of cichlid fauna such tools. Molecular information will be of equivalent to portions of the extinct species direct use in making decisions about fisheries of the large Lakes Kyoga and Victoria, has management and conservation practices. led us into speculation of a broader, and Therefore, interested parties in the LVR rather different role for satellite lakes than fishes, such as FISA and LVFO, will want to Greenwood had envisioned. Minor satellite foster such studies to allow the generation of lakes can act as refugia of the equivalent the knowledge base urgently needed to species in the big lakes. Satellite lakes conserve and manage fisheries biodiversity of generate species through allopatric isolation the LVR. We must all foster a greater and local selection regimes, but on a smaller understanding of the importance of this scale as the large lakes, while their sheltered genetic information for the future habitats offer protection (to species development and conservation of the LVR equivalent to those in the greater systems) fisheries, through education of fisheries from the drastic changes that the big lakes scientists and by encouraging the have been experiencing. We think small development of locally based genetic lakes have often been part of the ontogenetic research. speciation cycles of big lakes. Remembering that this is so may help explain some of the Satellite lakes versus large lakes faunal peculiarities of these systems. We are currently doing evolutionary analysis of these On the macroevolutionary level a recent discoveries using both morphological question of major interest has been the and molecular tools to elucidate the historical nature of satellite lakes. Are the evolutionary history of the two satellite lakes residual ponds left behind with interconnected systems (satellite lakes versus large portions of the diversity as the originally large lakes). expansive large lakes receded during extensive desiccation periods, or are they Further readings nursery beds for cichlid species that acted as lifeboats during periods of desiccation and Booton, G.C., L. Kaufman, M. Chandler, R. later fed their trapped fauna back into the Oguto-Ohwayo, W. Duan and P. Fuerst. large lakes? Of no doubt is the role these 1999. Evolution of the ribosomal RNA minor lakes are currently playing as refugia internal transcribed spacer one (ITS-1) in for endemic species ravaged by the dramatic cichlid fishes of the Lake Victoria region. Molecular Phylogenetics and Evolution 11: human impact in LVR since the turn of this 273-282. Lake Victoria cichlid fishes suggested by Duan, W., G.C. Booton, L. Kaufman, M. mitochondrial DNA sequences. Nature 347, Chandler and P.A. Fuerst. 1996. 550 - 553. Phylogenetic analysis of haplochromine Mwanja, W. 1996 Genetic variability and cichlid taxa utilizing DNA heteroduplex population structure of the tilapiine fauna of separation techniques. In: E.M. Donaldson the Lake Victoria basin (Uganda) in relation and D.D. MacKinlay (eds.), Aquaculture to exotic species introductions. Ohio State Biotechnology, Symposium Proceedings of University: MSc. thesis. the International Congress on the Biology of Mwanja, W., L. Kaufman, M. Chandler and P.A. Fishes, American Fisheries Society, p. 95- Fuerst. 1996. Population and stock 101. characterization of Lake Victoria tilapine Fryer, G. & Iles, T. D. (1972). The Cichlid fishes based on RAPD markers. In: E.M. Fishes of the Great Lakes of Africa. Their Donaldson and D.D. MacKinlay (eds.), Biology and Evolution. Edinburgh: Oliver & Aquaculture Biotechnology, Symposium Boyd. Proceedings of the International Congress on Fuerst, P., W. Mwanja, L. Kaufman and G. C. the Biology of Fishes, American Fisheries Booton. 1997. Genetic Phylogeography of Society, p. 115-124. introduced Oreochromis niloticus (Pisces: Mwanja, W., L. Kaufman, and P.A. Fuerst. 1996. Cichlidae) in Uganda. In: K. Fitzsimmons A note on recent advances in the genetic (ed.) TILAPIA AQUACULTURE; characterization of Tilapia stocks in Lake Proceedings of the Fourth International Victoria region. African Journal of Tropical Symposium on Tilapia in Aquaculture (ISTA Hydrobiology and Fisheries 6: 51-53. IV). Volume 1, pages 87-96, Northeast Ogutu-Ohwayo, R., R.E. Hecky, A.S. Cohen, and Regional Agricultural Engineering Service, L Kaufman. 1997. Human impacts on the Ithaca. African Great Lakes. Environmental Biology Greenwood, P.H. 1981. The Haplochromine of Fishes 50:117-131. Fishes of the East African Lakes. British Wu, L., G. C. Booton, L. S. Kaufman, M. Museum (Natural History), London, and Chandler, & P. A. Fuerst. 1996. Use of DNA Kraus International Publication, Munich. microsatellite loci to identify populations and IUCN (1990). 1990 IUCN Red List of species of Lake Victoria haplochromine Threatened Animals. IUCN Publications, cichlids. In: E. M. Donaldson & D. D. 192 pp. Geneva. Mackinlay (eds.), Aquaculture Johnson, T. C., C. A. Schulz, M. R. Talbot, K. Biotechnology, Symposium Proceedings of Kelts, R. D. Ricketts, G. Ngobi, K. the International Congress on Biology of Beuning, I. Ssemannda, & J. W. McGill. Fishes, American Fisheries Society, pp 105 - 1996. Late Pleistocene desiccation of Lake 114. Victoria and rapid evolution of cichlid fishes. Wu, L., L. Kaufman and P.A. Fuerst. 1999. Science 273: 1091-1093. Isolation of microsatellite markers in Kaufman 1992. Catastrophic change in Species- Astatoreochromis alluaudi and their cross Rich Freshwater Ecosystems. Bioscience, 42 species amplification in other African (11), 846-858 cichlids. Molecular Ecology 8: 895-897. Kaufman, L. S. 1997. 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