African cichlid fish: a model system in adaptive radiation research

Abstract

The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.

Figure 1

Frequency distribution of the age of African lacustrine cichlid fish radiations contrasted with approximate ages of other well-studied vertebrate adaptive radiations.

Figure 2

(a) The relationship between time for speciation (TFS) and radiation age calculated using 20 African cichlid radiations for which TFS was available (table 1 of electronic supplementary material). (b) The evolutionary species–area relationship for African cichlid radiations, calculated using 29 African cichlid radiations for which lake surface area and number of species were available (table 1 of electronic supplementary material). (c) The relationship between TFS and lake size calculated using 20 African cichlid radiations for which TFS and lake surface area were available (table 1 of electronic supplementary material). (d) The relationship between residual number of species (after the effect of lake size is taken into account) and radiation age, calculated using 20 African cichlid radiations for which both time in lake and lake surface area were available.

Figure 3

Species number through time plots for African cichlid radiations. (a) Several lineages of Lake Tanganyika cichlids (Limnochromini, Perissodini, Cyprichromini from Duftner et al. 2005; Bathybatini from Koblmueller et al. 2004, Ectodini from Koblmueller et al. 2005). (b) The radiation in Lake Barombi Mbo (Schliewen & Klee 2004).

Figure 4

(a) The ratios of number of successful radiations over number of ‘failed’ radiations mapped on a mitochondrial gene tree (ND2) for the African cichlid fish (tree from Klett & Meyer 2002). ‘Node 1’ corresponds to a hard polytomy deep in the African cichlid radiation, that has been interpreted as the signature of an adaptive radiation burst 14 Myr (ago) (Terai et al. 2003; figure 4b). ‘Node 2’ is a second major hard polytomy corresponding with the origin of the four deep lineages of Lake Tanganyika cichlids (Takahashi et al. 2001b). ‘Node 3’ is a third major hard polytomy corresponding to the radiation burst of the modern Lake Tanganyika lineage (Takahashi et al. 2001b; figure 4c). Note that several weakly supported nodes in this gene tree collapse to the same polytomy in multilocus trees (figure 4b,c). The different shading indicates sections of the tree that were compared for the ratio of successful to failed radiations. The light grey branch is the ‘East African’ lineage that emerged in the Tanganyika primary radiation, then radiated again in Lake Tanganyika, and much later seeded Lakes Malawi, Victoria, Makgadikgadi and many others (also figure 4c). Genera that were not sampled for this gene tree, but whose phylogenetic position is known from other mtDNA sequence data, are indicated in the ratio column. Note that the exact position of these does not affect the analysis because all of them are unambiguously assigned to one of the shaded branches. The origins of two proposed key evolutionary innovations, decoupled pharyngeal jaws (at the base of the tree) and egg dummies, are indicated. The third one, female mouthbrooding is not indicated because it evolved multiple times and is scattered throughout the tree. Abbreviations stand for lakes: Na=Natron; My=Manyara; Ji=Jipe; Cha=Chala; T=Tanganyika; V=Victoria; R=Rukwa; PM=Paleo–Makgadikgadi; M=Malawi; B=Bangweulu; Mw=Mweru; K=Kivu; E=Edward; A=Albert; C=Chad; Ki=Kinneret; Tu=Turkana; Ta=Tana; S=Stephanie; Ba=Barombi Mbo; Ej=Ejagham; U=Upemba; F=Fwa; Sa=Saka; Ns=Nshere; Lu=Lutoto; Ci=Chilwa; Nb=Nabugabo; Tm=Tumba; G=Guinas sink hole; Be=Bemin; Ko=Barombi ba Kotto; Nd=Mayi Ndombe. (b) A phylogenetic tree based on short interspersed element (SINE) insertion data. Each boxed number is a SINE locus, and arrowheads indicate their origins. The MVhL lineage is resolved in figure 4c. The grey circle at node 1 indicates the period when retention of ancestral polymorphisms (presence or absence of a SINE) was assumed to have occurred at loci 223, 260, 304, 316, 1223 and 1544. Reproduced with permission from Terai et al. 2003. (c) A phylogenetic tree for cichlid species in the 12 tribes of Lake Tanganyika, based on SINE insertion data. Arrowheads indicate internodes deduced from insertion of a SINE unit at each of 24 loci analysed. The three clades were supported by the patterns of insertion of a SINE unit at loci 213, 214, 245, 247, 254, 314, 455, 1569, 1666 and 1715 (the MVhL clade); at loci 328, 330, 343, 1221, 1238, 1262, 1269, 1277 and 1654 (the MVHT clade); and at loci 1233, 1265, 1281, 1291 and 1528 (the MVH clade). The grey portion of the tree indicates the period during which extensive putative incomplete lineage sorting of ancestral polymorphisms occurred (reproduced with permission from Takahashi et al. 2001b).