Old fossils-young species: Evolutionary history of an endemic gastropod assemblage in Lake Malawi

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1668, 2009, Pages 2837-2846

  Schultheiß, Roland ^a   Van Bocxlaer, Bert ^b   Wilke, Thomas ^a   Albrecht, Christian ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Ancient lake; Endemism; Environmental change; Fossil record; Lanistes; Molecular clock

Indexed keywords

MITOCHONDRIAL DNA;

ENDEMIC SPECIES; EVOLUTIONARY BIOLOGY; GASTROPOD; NICHE; SPECIATION (BIOLOGY);

ARTICLE; BIOLOGICAL TRAIT; COMPARATIVE STUDY; CONTROLLED STUDY; FOSSIL; GASTROPOD; GENETIC VARIABILITY; GENUS; HISTORY; INTROSPECTION; LAKE; LANISTES; MALAWI; MOLECULAR CLOCK; MOLECULAR EVOLUTION; MOLLUSC; NONHUMAN; PALEOENVIRONMENT; PHYLOGENY; PLEISTOCENE; PRIORITY JOURNAL; SPECIES;

AFRICA; EAST AFRICAN LAKES; LAKE MALAWI; SUB-SAHARAN AFRICA;

GASTROPODA; LANISTES;

EID: 67650888638     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.0467     Document Type: Article

References (91)

1. Ayala, F. J. 1997 Vagaries of the molecular clock. Proc. Natl Acad. Sci. USA 94, 7776-7783. (doi:10.1073/pnas.94.15.7776)
2. Barker, P. A., Leng, M. J., Gasse, F. & Huang, Y. 2007 Century-to-millennial scale climatic variability in Lake Malawi revealed by isotope records. Earth Planet. Sci. Lett. 261, 93-103. (doi:10.1016/j.epsl.2007.06.010)
3. Barnosky, A. D. 2001 Distinguishing the effects of the Red Queen and Court Jester on Miocene mammal evolution in the northern Rocky Mountains. J. Vert. Paleontol. 21, 172-185. (doi:10.1671/0272-4634(2001)021[0172: DTEOTR]2.0.CO;2)
4. Bennett, K. D. 2004 Continuing the debate on the role of Quaternary environmental change for macroevolution. Phil. Trans. R. Soc. Lond. B 359, 295-303. (doi:10.1098/rstb.2003.1395)
5. Benton, M. J. 2009 The Red Queen and the Court Jester: species diversity and the role of biotic and abiotic factors through time. Science 323, 728-732. (doi:10.1126/science.1157719)
6. Berthold, T. 1990a Intralacustrine speciation and the evolution of shell sculpture in gastropods of ancient lakes: application of Gü nther's niche concept. Abh. Naturwiss. Ver. Hamburg 31/32, 85-118.
7. Berthold, T. 1990b Phylogenetic relationships, adaptations and biogeographic origin of the Ampullariidae (Mollusca, Gastropoda) endemic to Lake Malawi. Abh. Naturwiss. Ver. Hamburg 31/32, 47-84.
8. Brown, F. H. & Feibel, C. S. 1991 Stratigraphy, depositional environments and paleogeography of the Koobi Fora Formation. In Koobi Fora Research Project, stratigraphy, artiodactyls and paleoenvironments, vol. 3 (ed. J. M. Harris), pp. 1-30. Oxford, UK: Clarendon Press.
9. Cohen, A. S., Lezzar, K.E., Tiercelin, J. J. & Soreghan, M.1997 New palaeogeographic and lake-level reconstructions of Lake Tanganyika: implications for tectonic, climatic and biological evolution in a rift lake. Basin Res. 9, 107-132. (doi:10.1046/j.1365-2117.1997.00038.x)
10. Cohen, A. S. et al. 2007 Ecological consequences of early Late Pleistocene megadroughts in tropical Africa. Proc. Natl Acad. Sci. USA 104, 16 422-16 427. (doi:10.1073/pnas.0703873104)
11. Colgan, D. J., Ponder, W. F., Beacham, E. & Macaranas, J. 2007 Molecular phylogenetics of Caenogastropoda (Gastropoda: Mollusca). Mol. Phylogen. Evol. 42, 717-737. (doi:10.1016/j.ympev.2006.10.009)
12. Crowley, T. E., Pain, T. & Woodward, F. R. 1964 A monographic review of the Mollusca of Lake Nyasa. Ann. Mus. r. Afr. Centr. Tervuren 88 Sci. Zool. 131, 1-58.
13. Day, J. J., Cotton, J. A. & Barraclough, T. G. 2008 Tempo and mode of diversification of Lake Tanganyika cichlid fishes. PLoS ONE 3, e1730. (doi:10.1371/journal.pone.0001730)
14. DeBusk, G. H. 1998 A 37,500-year pollen record from Lake Malaŵ i and implications for the biogeography of afromontane forests. J. Biogeogr. 25, 479-500. (doi:10.1046/j.1365-2699.1998.2530479.x)
15. Delvaux, D. 1995 Age of Lake Malawi (Nyasa) and water level fluctuations. Mus. R. Afr. Centr. Tervuren (Belg.) Dept. Geol. Min. Rapp. Ann. 1995-1996, 99-108.
16. Drummond, A. J. & Rambaut, A. 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214. (doi:10.1186/1471-2148-7-214)
17. Ebinger, C. J., Rosendahl, B. R. & Reynolds, D. J. 1987 Tectonic model of the Malawi rift, Africa. Tectonophysics 141, 215-235. (doi:10.1016/0040-1951(87)90187-9)
18. Ebinger, C. J., Deino, A. L., Drake, R. E. & Tesha, A. L. 1989 Chronology of volcanism and rift basin propagation: Rungwe Volcanic Province, East Africa. J. Geophys. Res. 94, 15 785-15 803. (doi:10.1029/JB094iB11p15785)
19. Edwards, S. V. & Beerli, P. 2000 Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54, 1839-1854. (doi:10.1111/j.0014-3820.2000. tb01231.x)
20. Felsenstein, J. 1988 Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22, 521-565. (doi:10.1146/annurev. ge.22.120188.002513)
21. Finney, B. P., Scholz, C. A., Johnson, T. C., Trumbore, S. & Southon, J. 1996 Late Quaternary lake-level changes of Lake Malawi. In The limnology, climatology and paleoclimatology of the East African Lakes (eds T. C. Johnson & E. O. Odada), pp. 495-508. Amsterdam, UK: Gordon and Breach Scientific Publishers.
22. Folmer, O., Black, M., Hoeh, W. R., Lutz, R. & Vrijenhoek, R. 1994 DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294-299.
23. Fryer, G. 1959 The trophic interrelationships and ecology of some littoral communities of Lake Nyasa with especial reference to the fishes, and a discussion of the evolution of a group of rock-frequenting Cichlidae. Proc. Zool. Soc. Lond. 132, 153-281.
24. Genner, M. J. & Turner, G. F. 2005 The mbuna cichlids of Lake Malawi: a model for rapid speciation and adaptive radiation. Fish Fish. 6, 1-34. (doi:10.1111/j.1467-2679.2005.00173.x)
25. Genner, M. J., Nichols, P., Carvalho, G. R., Robinson, R. L., Shaw, P.W., Smith, A. & Turner, G. F. 2007a Evolution of a cichlid fish in a Lake Malawi satellite lake. Proc. R. Soc. B 274, 2249-2257. (doi:10.1098/rspb.2007.0619)
26. Genner, M. J., Todd, J.A., Michel, E., Erpenbeck, D., Jimoh, A., Joyce, D. A., Piechocki, A. & Pointier, J. P. 2007b Amassing diversity in an ancient lake: evolution of a morphologically diverse parthenogenetic gastropod assemblage inLakeMalawi. Mol. Ecol. 16, 517-530. (doi:10.1111/j.1365-294X.2006.03171.x)
27. Guindon, S. & Gascuel, O. 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704. (doi:10.1080/10635150390235520)
28. Hall, T. A. 1999 BIOEDIT: a user-friendly biological sequence alignment editor and analysis program for WINDOWS 95/98/NT. Nucl. Acids Symp. Ser. 41, 95-98.
29. Hauswald, A.-K., Albrecht, C. & Wilke, T. 2008 Testing two contrasting evolutionary patterns in ancient lakes: species flock vs. species scatter in valvatid gastropods of Lake Ohrid. Hydrobiologia 615, 169-179. (doi:10.1007/s10750-008-9556-0)
30. Hillis, D. M., Mable, B. K. & Moritz, C. 1996 Applications of molecular systematics. In Molecular systematics (eds D. M. Hillis, C. Moritz & B. K. Mable), pp. 515-543. Sunderland, MA: Sinauer Associates, Inc.
31. Ho, S. Y.W. & Larson, G. 2006 Molecular clocks: when times are a-changin. Trends Genet. 22, 79-83. (doi:10.1016/j.tig.2005.11. 006)
32. Huelsenbeck, J. P. & Ronquist, F. 2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755. (doi:10.1093/bioinformatics/17.8.754)
33. Huelsenbeck, J. P., Larget, B. & Swofford, D. 2000 A compound Poisson process for relaxing the molecular clock. Genetics 154, 1879-1892.
34. Johnson, T. C., Scholz, C. A., Talbot, M. R., Kelts, K., Ricketts, R. D., Ngobi, G., Beuning, K., Ssemmanda, I. & McGill, J. W. 1996 Late Pleistocene desiccation of Lake Victoria and rapid evolution of cichlid fishes. Science 273, 1091-1093. (doi:10.1126/science.273.5278.1091)
35. Jørgensen, A., Kristensen, T. K. & Madsen, H. 2008 A molecular phylogeny of apple snails (Gastropoda, Caenogastropoda, Ampullariidae) with an emphasis on African species. Zool. Scr. 37, 245-252. (doi:10.1111/j.1463-6409.2007.00322.x)
36. Kadmon, R. & Benjamini, Y. 2006 Effects of productivity and disturbance on species richness: a neutral model. Am. Nat. 167, 939-946. (doi:10.1086/504602)
37. Kishino, H., Thorne, J. L. & Bruno, W. J. 2001 Performance of a divergence time estimation method under a probabilistic model of rate evolution. Mol. Biol. Evol. 18, 352-361.
38. Knowles, L. L. & Carstens, B. C. 2007 Delimiting species without monophyletic gene trees. Syst. Biol. 56, 887-895. (doi:10.1080/10635150701701091)
39. Kocher, T. D. 2004 Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Genet. 5, 288-298. (doi:10.1038/nrg1316)
40. Kondoh, M. 2001 Unifying the relationships of species richness to productivity and disturbance. Proc. R. Soc. Lond. B 268, 269-271. (doi:10.1098/rspb.2000.1384)
41. Kullmer, O. 2008 The fossil suidae from the Plio-Pleistocene Chiwondo Beds of northern Malawi, Africa. J. Vert. Paleontol. 28, 208-216. (doi:10.1671/0272-4634(2008)28[208:TFSFTP]2.0.CO;2)
42. Landan, G. & Graur, D. 2007 Heads or tails: a simple reliability check for multiple sequence alignments. Mol. Biol. Evol. 24, 1380-1383. (doi:10.1093/molbev/msm060)
43. Louda, S. M. & McKaye, K. R. 1982 Diurnal movements in populations of the prosobranch Lanistes nyassanus at Cape Maclear, Lake Malawi, Africa. Malacologia 23, 13-21.
44. Louda, S. M., McKaye, K. R., Kocher, T. D. & Stackhouse, C. J. 1984 Activity, dispersion, and size of Lanistes nyassanus and L. solidus (Gastropoda, Ampullariidae) over the depth gradient at Cape Maclear, Lake Malawi, Africa. Veliger 26, 145-152.
45. Macdonald, K. S., Yampolsky, L. & Duffy, J. E. 2005 Molecular and morphological evolution of the amphipod radiation of Lake Baikal. Mol. Phylogen. Evol. 35, 323-343. (doi:10.1016/j.ympev.2005.01.013)
46. Mandahl-Barth, G. 1972 The freshwater Mollusca of Lake Malawi. Rev. Zool. Bot. Afr. 86, 257-289.
47. Marijnissen, S. A. E., Michel, E., Daniels, S. R., Erpenbeck, D., Menken, S. B. J. & Schram, F. R. 2006 Molecular evidence for recent divergence of Lake Tanganyika endemic crabs (Decapoda: Platythelphusidae). Mol. Phylogen. Evol. 40, 628-634. (doi:10.1016/j.ympev.2006.03.025)
48. Martens, E. V. 1897 Beschalte Weichthiere Ost-Afrikas. In Deutsch-Ost-Afrika, vol. 4 (ed. F. Stuhlmann), pp. 1-308. Berlin, Germany: Dietrich Reimer.
49. Martens, K. 1994 Speciation in ancient lakes: 40 years after Brooks. Arch. Hydrobiol. Beih. 44, 75-96.
50. Martens, K. 2002 Redundancy and ecosystem stability in the fluctuating environments of long-lived lakes. In The East African Great Lakes: limnology, palaeolimnology and biodiversity, vol. 12 (ed. E. O. Odada & D. O. Olago), pp. 309-319. Dordrecht, The Netherlands: Academic Publishers.
51. Martens, K. 2003 On the evolution of Gomphocythere (Crustacea, Ostracoda) in Lake Nyassa/Malawi (East Africa), with the description of 5 new species. Hydrobiologia 497, 121-144. (doi:10.1023/A:1025417822555)
52. Michel, E. 1994 Why snails radiate: a review of gastropod evolution in long-lived lakes, both recent and fossil. Arch. Hydrobiol. Beih. 44, 285-317.
53. Owen, R. B., Crossley, R., Johnson, T. C., Tweddle, D., Kornfield, I., Davison, S., Eccles, D. H. & Engstrom, D. E. 1990Major lowlevels of Lake Malawi and their implications for speciation rates in cichlid fishes. Proc. R. Soc. Lond. B 240, 519-553. (doi:10.1098/rspb.1990.0052)
54. Palacios-Fest, M. R., Alin, S. R., Cohen, A. S., Tanner, B. & Heuser, H. 2005 Paleolimnological investigations of anthropogenic environmental change in Lake Tanganyika. IV. Lacustrine paleoecology. J. Paleolimn. 34, 51-71. (doi:10.1007/s10933-005-2397-1)
55. Palumbi, S., Martin, A., Romano, S., Mcmillian, W. O., Stice, L. & Grabowski, G. 1991 The simple fool's guide to PCR. Honolulu, HI: University of Hawaii.
56. Paradis, E., Claude, J. & Strimmer, K. 2004 APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289-290. (doi:10.1093/bioinformatics/btg412)
57. Peters, S. E. 2008 Environmental determinants of extinction selectivity in the fossil record. Nature 454, 626-629. (doi:10.1038/ nature07032)
58. Pulquério, M. J. F. & Nichols, R. A. 2007 Dates from the molecular clock: how wrong can we be? Trends Ecol. Evol. 22, 180-184. (doi:10.1016/j.tree.2006.11.013)
59. R Development Core Team 2007 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
60. Ring, U. & Betzler, C. 1995 Geology of the Malawi Rift: kinematic and tectonosedimentary background to the Chiwondo Beds, Northern Malawi. J. Hum. Evol. 28, 7-21. (doi:10.1006/jhev.1995.1003)
61. Sanders, H. L. 1968 Marine benthic diversity: a comparative study. Am. Nat. 102, 243-282. (doi:10.1086/282541)
62. Sanderson, M. J. 1997 A nonparametric approach to estimating divergence times in the absence of rate constancy. Mol. Biol. Evol. 14, 1218-1231.
63. Schluter, D. 2000 The ecology of adaptive radiation. Oxford series in ecology and evolution. Oxford, UK: Oxford University Press.
64. Scholz, C. A. & Rosendahl, B. R. 1988 Low lake stands in lakes Malawi and Tanganyika, East Africa, delineated with multifold seismic data. Science 240, 1645-1648. (doi:10. 1126/science.240.4859.1645)
65. Scholz, C. A. et al. 2007 East African megadroughts between 135 and 75 thousand years ago and bearing on earlymodern human origins. Proc. Natl Acad. Sci. USA 104, 16 416-16 421. (doi:10.1073/pnas.0703874104)
66. Schön, I. & Martens, K. 2004 Adaptive, pre-adaptive and non-adaptive components of radiations in ancient lakes: a review. Org. Divers. Evol. 4, 137-156. (doi:10.1016/j.ode.2004.03.001)
67. Schrenk, F., Bromage, T. G., Gorthner, A. & Sandrock, O. 1995 Paleoecology of the Malawi Rift: vertebrate and invertebrate faunal contexts of the Chiwondo Beds, northern Malawi. J. Hum. Evol. 28, 59-70. (doi:10. 1006/jhev.1995.1006)
68. Schultheiß, R., Albrecht, C., Bößneck, U. & Wilke, T. 2008 The neglected side of speciation in ancient lakes: phylogeography of an inconspicuous mollusc taxon in lakes Ohrid and Prespa. Hydrobiologia 615, 141-156. (doi:10.1007/s10750-008-9553-3)
69. Seehausen, O. 2006 African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. B 273, 1987-1998. (doi:10.1098/rspb.2006.3539)
70. Seehausen, O., Takimoto, G., Roy, D. & Jokela, J. 2008 Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol. Ecol. 17, 30-44. (doi:10.1111/j.1365-294X.2007.03529.x)
71. Sherbakov, D. Y. 1999 Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal. Trends Ecol. Evol. 14, 92-95. (doi:10.1016/S0169-5347(98)01543-2)
72. Spigel, R. H. & Coulter, G. W. 1996 Comparison of hydrology and physical limnology of the East African Great Lakes: Tanganyika, Malawi, Victoria, Kivu and Turkana (with references to some North American great lakes). In The limnology, climatology and paleoclimatology of the East African Lakes (eds T. C. Johnson & E. O. Odada), pp. 103-140. Amsterdam, UK: Gordon and Breach Scientific Publishers.
73. Stager, J. C. & Johnson, T. 2008 The late Pleistocene desiccation of Lake Victoria and the origin of its endemic biota. Hydrobiologia 596, 5-16. (doi:10.1007/s10750-007-9158-2)
74. Stamatakis, A., Hoover, P. & Rougemont, J. 2008 A rapid bootstrap algorithm for the RAXML Web Servers. Syst. Biol. 57, 758-771. (doi:10.1080/10635150802429642)
75. Sturmbauer, C., Baric, S., Salzburger, W., Ruber, L. & Verheyen, E. 2001 Lake level fluctuations synchronize genetic divergences of cichlid fishes in African lakes. Mol. Biol. Evol. 18, 144-154.
76. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994 CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680. (doi:10.1093/nar/22.22. 4673)
77. Turner, G. F. 2007 Adaptive radiation of cichlid fish. Curr. Biol. 17, R827-R831. (doi:10.1016/j.cub.2007.07.026)
78. Van Bocxlaer, B. 2005 Changes in the malacofauna of Lake Malawi since mid-Holocene times. Geol. Belg. 8, 124.
79. Van Bocxlaer, B., Van Damme, D. & Feibel, C. S. 2008 Gradual versus punctuated equilibrium evolution in the Turkana basin molluscs: evolutionary events or biological invasions? Evolution 62, 511-520. (doi:10.1111/j.15585646.2007.00296.x)
80. Van Damme, D. 1984 The freshwater Mollusca of northern Africa. Distribution, biogeography and palaeoecology. Developments in hydrobiology. Dordrecht, The Netherlands: Dr W. Junk Publishers.
81. Van Damme, D. & Pickford, M. 1995 The late Cenozoic Ampullariidae (Mollusca, Gastropoda) of the Albertine Rift Valley (Uganda-Zaire). Hydrobiologia 316, 1-32. (doi:10.1007/BF00019372)
82. Van Neer, W. 1994 Cenozoic fish fossils from the Albertine Rift Valley in Uganda. In Geology and palaeobiology of the Albertine Rift Valley, Uganda-Zaire, vol. II Palaeobiology Palaeobiology (eds B. Senut & M. Pickford), pp. 89-127. Milwaukee, WI: CIFEG Occasional Publications.
83. Verheyen, E., Ruber, L., Snoeks, J. & Meyer, A. 1996 Mitochondrial phylogeography of rock-dwelling cichlid fishes reveals evolutionary influence of historical lake level fluctuations of Lake Tanganyika, Africa. Phil. Trans. R. Soc. Lond. B 351, 797-805. (doi:10.1098/rstb.1996.0074)
84. Verheyen, E., Salzburger, W., Snoeks, J. & Meyer, A. 2003 Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300, 325-329. (doi:10.1126/science.1080699)
85. Welch, J. J. & Bromham, L. 2005 Molecular dating when rates vary. Trends Ecol. Evol. 20, 320-327. (doi:10.1016/j.tree.2005.02.007)
86. Wilke, T. 2003 Salenthydrobia gen. nov (Rissooidea: Hydrobiidae): a potential relict of the Messinian salinity crisis. Zool. J. Linn. Soc. 137, 319-336. (doi:10.1046/j.1096-3642.2003.00049.x)
87. Wilke, T. 2004 How dependable is a non-local molecular clock? A reply to Hausdorf et al. (2003). Mol. Phylogen. Evol. 30, 835-840. (doi:10.1016/j.ympev.2003.08.008)
88. Wilke, T., Davis, G. M., Qiu, D. C. & Spear, R. C. 2006 Extreme mitochondrial sequence diversity in the intermediate schistosomiasis host Oncomelania hupensis robertsoni: another case of ancestral polymorphism? Malacologia 48, 143-157.
89. Wilke, T., Schultheiß, R. & Albrecht, C. In press. As time goes by: a simple fool's guide to molecular clock approaches in invertebrates. Am. Malacol. Bull.
90. Wilson, A. B., Glaubrecht, M. & Meyer, A. 2004 Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika. Proc. R. Soc. Lond. B 271, 529-536. (doi:10.1098/rspb.2003.2624)
91. Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. 2003 An index of substitution saturation and its application. Mol. Phylogen. Evol. 26, 1-7. (doi:10.1016/S1055-7903(02)00326-3)