Parallel life history evolution in mouthbrooding cichlids from the African Great Lakes Fabrice Duponchelle*†‡§, Emmanuel Paradis†, Anthony J. Ribbink*¶, and George F. Turnerʈ *Southern African Development Conference/Global Environment Facility, Lake Malawi Biodiversity Conservation Project, P.O. Box 311 Salima, Malawi; †Institut de Recherche pour le De´veloppement (UR 175)/GAMET, BP 5095, 34196 Montpellier Cedex 1, France; ¶South African Institute for Aquatic Biodiversity, P Bag 1015, Grahamstown 6140, South Africa; and ʈSchool of Biological Sciences, Bangor University, Bangor LL57 2UW, Wales, United Kingdom Edited by John C. Avise, University of California, Irvine, CA, and approved August 20, 2008 (received for review March 7, 2008) The existence of ancient deep-water lakes provides an opportunity exceptional for pelagic teleost fish. Unusually, all known cichlid to study the independent adaptation of aquatic organisms to species provide parental care of eggs and young. Many species are pelagic, benthic, and rocky shore habitats. With improving reso- biparental substrate-spawners, whose eggs and young are guarded lution of their phylogenetic relationships, the many cichlid fish by both parents. Many other species are maternal mouthbrooders, species endemic to the African Great Lakes Malawi, Tanganyika, in which females pick up and brood eggs and larvae for a few weeks, and Victoria provide a significant resource for the comparative with some species even allowing independently feeding young to study of such evolutionary processes. Here, we show that cichlid return to the mouth when they are threatened with predation (17, lineages colonizing rocky shores and pelagic habitats in the dif- 23). All cichlid species from Lake Victoria and all except one from ferent lakes have independently evolved larger eggs and lower Lake Malawi are maternal mouthbrooders. Although nearly every fecundities than benthic lineages, suggesting parallel adaptive type of parental care is represented in Lake Tanganyika, all pelagic life-history evolution. By contrast, other pelagic teleost fishes in species and many of the rocky shore and benthic species are both marine and freshwater habitats, including African lakes, mouthbrooders [supporting information (SI) Table S1 and SI Text]. typically produce large numbers of very small eggs. Our results also Mouthbrooders typically produce fewer, larger eggs than substrate suggest that decreased fecundity and increased egg size not only spawners (17), and therefore, to avoid the confounding effect of the occurred independently in each lake but occurred independently in type of parental care on the ecological correlates of life-history the colonization of rocky and pelagic habitats. strategies, all species included in this study are mouthbrooders. We compared batch fecundities and egg sizes of cichlid fishes from parallelism ͉ phylogenetically controlled comparative analysis ͉ phylogeny pelagic, benthic, and rocky-shore habitats in all three lakes using new and published data. We adopted a two-step approach for data lucidating whether similar ecological specializations in closely analysis: first, testing for significant effects on the life-history traits Erelated lineages are the result of unique or repeated evolution- with linear models and then assessing whether significant effects ary events is of particular interest in the understanding of adaptive were confounded by phylogenetic nonindependence among species evolution (1, 2). The demonstration of parallel evolution of closely (24). The second step required the estimation of a phylogeny for the related yet phylogenetically distinct lineages in similar environ- species included in our dataset. The phylogeny of the Victorian ments provides strong evidence of evolution driven by natural cichlids is still poorly resolved (25), and DNA sequences were selection because genetic drift is unlikely to produce repeated available for few species for which we had life-history data. For evolution in the same direction (3, 4). Instances of parallelism Lakes Malawi and Tanganyika, we used comparative methods to abound in animal evolution (5), but most cases refer to morpho- account for the effect of phylogenetic relationships on life-history logical traits such as in cave amphipods (6–8), Anolis lizards (9), or correlations (26, 27) and Markovian models to reconstruct evolu- lake whitefish (10). Examples of repeated evolution of the same tionary transitions among habitats (28). life-history traits are scarcer, although a convincing case has been made for independent adaptations to predator-mediated mortality Results in several populations of Trinidadian guppies (11). To build such a Fecundities differed significantly among habitats and lakes (Fig. 1A case, one needs to demonstrate that multiple populations or species and Table 1), but the lack of a significant interaction indicated exposed to similar environments have evolved similar traits inde- similar contrasts among habitats in all three lakes. Controlling for pendently in different localities and evidence that the similarities phylogeny (Fig. 2A), the difference among lakes was no longer among populations are the product of the same sort of natural significant, which was expected because the haplochromine species selection (11). flocks of lakes Malawi and Victoria represent independent colo- The cichlid fishes of the East African Great Lakes represent an nizations (14), but the habitat effect remained significant. In the ideal model for the study of parallel evolution. An estimated analysis without phylogenetic correction, egg diameter varied sig- 660–1,319 species of cichlid fishes have been recorded from Lakes nificantly among both habitats and lakes (Fig. 1B and Table 1), but Malawi, Tanganyika, and Victoria, most endemic to a single lake again, the difference among lakes was confounded with phylogeny catchment (12). These species flocks are so rich that, collectively, (Fig. 2B). A significant interaction term, even after phylogenetic they provide the best example of rapid adaptive radiation in correction (Fig. 2B), indicated that the contrast among habitats was vertebrates (13–16). The independent radiations (14, 15) in the three lakes have produced very similar communities. Many of these species are habitat specialists, with most of them confined either to Author contributions: F.D. and A.J.R. designed research; F.D. performed research; F.D., E.P., rocky shores or to sand/mud bottoms (benthic), whereas a few are and G.F.T. analyzed data; and F.D., E.P., A.J.R., and G.F.T. wrote the paper. found in open water (pelagic) habitats (17). There are several well The authors declare no conflict of interest. documented examples of parallel evolution of morphology associ- This article is a PNAS Direct Submission. ated with independent colonization of similar habitats (18–20) as ‡Present address: 357 Calle Teruel, Miraflores, Lima 18, Peru. well as parallel evolution of coloration (21, 22). Here, we show that §To whom correspondence should be addressed. E-mail: [email protected]. parallel evolution of habitat specialization in East African Great This article contains supporting information online at www.pnas.org/cgi/content/full/ EVOLUTION Lake cichlids is further accompanied by hitherto undocumented 0802343105/DCSupplemental. parallel evolution of life-history traits and by a reproductive strategy © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0802343105 PNAS ͉ October 7, 2008 ͉ vol. 105 ͉ no. 40 ͉ 15475–15480 Downloaded by guest on September 30, 2021 ) 8000 8 Habitat Lake -1 A B A 7000 Benthic 7 6000 Pelagic 6 5000 Rock 4000 5 Frequency Frequency 3000 4 2000 0 50 100 150 0 204060 3 Egg (mm) diameter 1000 0.0 0.1 0.2 0.3 0.4 0.0 0.2 0.4 0.6 0.8 1.0 Relative fecundity (eggs.kg fecundity Relative 0 2 P values P values Tanganyika Malawi Victoria Tanganyika Malawi Victoria log(body mass) 8 2600 C ) 3 2200 7 .10 -1 1800 6 1400 Frequency 1000 5 050100150 600 4 0.00 0.10 0.20 0.30 200 P values 3 Egg diameter (mm) 5 Habitat Lake 4 2 B Relative fecundity (eggs.kg fecundity Relative 3 2 1 1 0 0 Frequency Frequency 0103050 020 60 100 Victoria (6) Victoria Malawi (12) Clupeidae (6) Clupeidae 0.0 0.2 0.4 0.6 0.0 0.2 0.4 0.6 0.8 1.0 Tanganyika (4) Lates stappersi Engraulidae (9) Scombridae (15) Leiognathidae (1) Leiognathidae Dussumieriidae (2) Dussumieriidae P values P values Limnothrissa miodon Engraulicypris sardella Stolothrissa tanganicae Rastrineobola argentea log(body mass) Habitat*Lake Marine Great lakes Great lakes pelagics non-cichlid pelagics pelagic cichlids Fig. 1. Pelagic cichlid fishes have lower fecundities (A) and larger eggs (B) than benthic and rocky shore cichlid fishes from the same lake, and (C) pelagic fishes of other families. Shown are means and standard errors, with the number of species in brackets. Data sources are in SI Text. Frequency Frequency 0204060 050100150 different between lakes. Egg size differences among habitats were 0.00 0.04 0.08 0.12 0.0 0.2 0.4 0.6 greatest in Tanganyika and least in Victoria (Fig. 1B). P values P values In all three lakes, pelagic species had the lowest fecundities and Fig. 2. Histograms of the P values from the GEE-based phylogenetically con- largest eggs, whereas benthic species had the highest fecundities and trolled comparative analyses for clutch size (A) and oocyte diameter (B). The smallest eggs (Fig. 1 A and B). Rock-dwelling species showed comparative analyses were repeated for the 200 bootstrap trees to assess intermediate