Hybridization among littoral cichlid species in Lake Tanganyika was inferred in several molecular phylogenetic studies. The phenomenon is generally attributed to the lake level-induced shoreline and habitat changes. These allow for allopatric divergence of geographically fragmented populations alternating with locally restricted secondary contact and introgression between incompletely isolated taxa. In contrast, the deepwater habitat is characterized by weak geographic structure and a high potential for gene flow, which may explain the lower species richness of deepwater than littoral lineages. For the same reason, divergent deepwater lineages should have evolved strong intrinsic reproductive isolation already in the incipient stages of diversification, and, consequently, hybridization among established lineages should have been less frequent than in littoral lineages. We test this hypothesis in the endemic Lake Tanganyika deepwater cichlid tribe Bathybatini by comparing phylogenetic trees of Hemibates and Bathybates species obtained with nuclear multilocus AFLP data with a phylogeny based on mitochondrial sequences. Consistent with our hypothesis, largely congruent tree topologies and negative tests for introgression provided no evidence for introgressive hybridization between the deepwater taxa. Together, the nuclear and mitochondrial data established a well-supported phylogeny and suggested ecological segregation during speciation. 1. Introduction Cichlid fishes have undergone spectacular radiations in different parts of the world. In particular, the species flocks of the East African Great Lakes are well-known examples for rapid evolution and speciation [1–5]. Each of the three Great Lakes—Tanganyika, Malawi, and Victoria—is inhabited by hundreds of mostly endemic cichlid species [6, 7]. Notably, most of the diversity is found in the littoral habitat, whereas reduced species richness in the deep benthal and pelagial seems to be a common phenomenon in all East African Great Lakes [7–10]. At least three factors may have contributed to this pattern: (i) reduced niche diversity in the pelagic and in deepwater benthic zones, (ii) a narrow ambient light spectrum consisting only of short-wavelength blue light and hence less promotive of diversification mechanisms contingent on color perception than the shallow clear-water habitats [11–14], and (iii) the absence of strong barriers to gene flow. Indeed, deepwater cichlid species often have lake-wide distributions with very low, if any, population genetic structure over large geographic distances [10, 15, 16]
References
[1]
D. Schluter, The Ecology of Adaptive Radiation, Oxford University Press, Oxford, UK, 2000.
[2]
T. D. Kocher, “Adaptive evolution and explosive speciation: the cichlid fish model,” Nature Reviews Genetics, vol. 5, no. 4, pp. 288–298, 2004.
[3]
G. F. Turner, “Adaptive radiation of cichlid fish,” Current Biology, vol. 17, no. 19, pp. R827–R831, 2007.
[4]
W. Salzburger, “The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes,” Molecular Ecology, vol. 18, no. 2, pp. 169–185, 2009.
[5]
C. Sturmbauer, M. Husemann, and P. Danley, “Explosive speciation and adaptive radiation in East African cichlid fishes,” in Biodiversity Hotspots, F. E. Zachos and J. C. Habel, Eds., pp. 333–362, Springer, Berlin, Germany, 2011.
[6]
G. F. Turner, O. Seehausen, M. E. Knight, C. J. Allender, and R. L. Robinson, “How many species of cichlid fishes are there in African lakes?” Molecular Ecology, vol. 10, no. 3, pp. 793–806, 2001.
[7]
S. Koblmüller, K. M. Sefc, and C. Sturmbauer, “The Lake Tanganyika cichlid species assemblage: recent advances in molecular phylogenetics,” Hydrobiologia, vol. 615, no. 1, pp. 5–20, 2008.
[8]
G. F. Turner, Offshore Cichlids of Lake Malawi, Cichlid Press, Lauenau, Germany, 1996.
[9]
O. Seehausen, F. Witte, E. F. Katunzi, J. Smits, and N. Bouton, “Patterns of the remnant cichlid fauna in southern Lake Victoria,” Conservation Biology, vol. 11, no. 4, pp. 890–904, 1997.
[10]
P. W. Shaw, G. F. Turner, M. R. Idid, R. L. Robinson, and G. R. Carvalho, “Genetic population structure indicates sympatric speciation of Lake Malawi pelagic cichlids,” Proceedings of the Royal Society B, vol. 267, no. 1459, pp. 2273–2280, 2000.
[11]
O. Seehausen, J. J. M. van Alphen, and F. Witte, “Cichlid fish diversity threatened by eutrophication that curbs sexual selection,” Science, vol. 277, no. 5333, pp. 1808–1811, 1997.
[12]
O. Seehausen, J. J. M. van Alphen, and R. Lande, “Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection,” Ecology Letters, vol. 2, no. 6, pp. 367–378, 1999.
[13]
M. E. Knight and G. F. Turner, “Laboratory mating trials indicate incipient speciation by sexual selection among populations of the cichlid fish Pseudotropheus zebra from Lake Malawi,” Proceedings of the Royal Society B, vol. 271, no. 1540, pp. 675–680, 2004.
[14]
M. E. Maan, O. Seehausen, L. S？derberg et al., “Intraspecific sexual selection on a speciation trait, male coloration, in the Lake Victoria cichlid Pundamilia nyererei,” Proceedings of the Royal Society B, vol. 271, no. 1556, pp. 2445–2452, 2004.
[15]
M. J. Genner, P. Nichols, P. W. Shaw, G. R. Carvalho, R. L. Robinson, and G. F. Turner, “Genetic homogeneity among breeding grounds and nursery areas of an exploited Lake Malawi cichlid fish,” Freshwater Biology, vol. 53, no. 9, pp. 1823–1831, 2008.
[16]
M. J. Genner, P. Nichols, P. W. Shaw, G. R. Carvalho, R. L. Robinson, and G. F. Turner, “Population structure on breeding grounds of Lake Malawi's “twilight zone” cichlid fishes,” Journal of Biogeography, vol. 37, no. 2, pp. 258–269, 2010.
[17]
L. Hauser, G. R. Carvalho, and T. J. Pitcher, “Genetic population structure in the Lake Tanganyika sardine Limnothrissa miodon,” Journal of Fish Biology, vol. 53, Supplement A, pp. 413–429, 1998.
[18]
L. Kuusipalo, “Genetic differentiation of endemic nile perch Lates stappersi (Centropomidae, Pisces) populations in Lake Tanganyika suggested by RAPD markers,” Hydrobiologia, vol. 407, pp. 141–148, 1999.
[19]
M. J. H. van Oppen, G. F. Turner, C. Rico et al., “Unusually fine-scale genetic structuring found in rapidly speciating Malawi cichlid fishes,” Proceedings of the Royal Society of London Series B, vol. 264, no. 1289, pp. 1803–1812, 1997.
[20]
M. E. Arnegard, J. A. Markert, P. D. Danley, J. R. Stauffer, A. J. Ambali, and T. D. Kocher, “Population structure and colour variation of the cichlid fish Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi,” Proceedings of the Royal Society B, vol. 266, no. 1415, pp. 119–130, 1999.
[21]
J. A. Marker, M. E. Arnegard, P. D. Danley, and T. D. Kocher, “Biogeography and population genetics of the Lake Malawi cichlid Melanochromis auratus: habitat transience, philopatry and speciation,” Molecular Ecology, vol. 8, no. 6, pp. 1013–1026, 1999.
[22]
P. D. Danley, J. A. Markert, M. E. Arnegard, and T. D. Kocher, “Divergence with gene flow in the rock-dwelling cichlids of Lake Malawi,” Evolution, vol. 54, no. 5, pp. 1725–1737, 2000.
[23]
M. I. Taylor, L. Rüber, and E. Verheyen, “Microsatellites reveal high levels of population substructuring in the species-poor Eretmodine cichlid lineage from Lake Tanganyika,” Proceedings of the Royal Society B, vol. 268, no. 1469, pp. 803–808, 2001.
[24]
C. Rico and G. F. Turner, “Extreme microallopatric divergence in a cichlid species from Lake Malawi,” Molecular Ecology, vol. 11, no. 8, pp. 1585–1590, 2002.
[25]
N. Duftner, K. M. Sefc, S. Koblmüller et al., “Distinct population structure in a phenotypically homogeneous rock-dwelling cichlid fish from Lake Tanganyika,” Molecular Ecology, vol. 15, no. 9, pp. 2381–2395, 2006.
[26]
N. Duftner, K. M. Sefc, S. Koblmüller, W. Salzburger, M. Taborsky, and C. Sturmbauer, “Parallel evolution of facial stripe patterns in the Neolamprologus brichardi/pulcher species complex endemic to Lake Tanganyika,” Molecular Phylogenetics and Evolution, vol. 45, no. 2, pp. 706–715, 2007.
[27]
S. Koblmüller, K. M. Sefc, N. Duftner, M. Warum, and C. Sturmbauer, “Genetic population structure as indirect measure of dispersal ability in a Lake Tanganyika cichlid,” Genetica, vol. 130, no. 2, pp. 121–131, 2007.
[28]
S. Koblmüller, W. Salzburger, B. Obermüller, E. Eigner, C. Sturmbauer, and K. M. Sefc, “Separated by sand, fused by dropping water: habitat barriers and fluctuating water levels steer the evolution of rock-dwelling cichlid populations in Lake Tanganyika,” Molecular Ecology, vol. 20, no. 11, pp. 2272–2290, 2011.
[29]
K. M. Sefc, S. Baric, W. Salzburger, and C. Sturmbauer, “Species-specific population structure in rock-specialized sympatric cichlid species in Lake Tanganyika, East Africa,” Journal of Molecular Evolution, vol. 64, no. 1, pp. 33–49, 2007.
[30]
C. E. Wagner and A. R. McCune, “Contrasting patterns of spatial genetic structure in sympatric rock-dwelling cichlid fishes,” Evolution, vol. 63, no. 5, pp. 1312–1326, 2009.
[31]
N. Konijnendijk, D. A. Joyce, H. D. J. Mrosso, M. Egas, and O. Seehausen, “Community genetics reveal elevated levels of sympatric gene flow among morphologically similar but not among morphologically dissimilar species of Lake Victoria cichlid fish,” International Journal of Evolutionary Biology, vol. 2011, Article ID 616320, 12 pages, 2011.
[32]
L. Rüber, A. Meyer, C. Sturmbauer, and E. Verheyen, “Population structure in two sympatric species of the Lake Tanganyika cichlid tribe Eretmodini: evidence for introgression,” Molecular Ecology, vol. 10, no. 5, pp. 1207–1225, 2001.
[33]
W. Salzburger, S. Baric, and C. Sturmbauer, “Speciation via introgressive hybridization in East African cichlids?” Molecular Ecology, vol. 11, no. 3, pp. 619–625, 2002.
[34]
B. Egger, S. Koblmüller, C. Sturmbauer, and K. M. Sefc, “Nuclear and mitochondrial data reveal different evolutionary processes in the Lake Tanganyika cichlid genus Tropheus,” BMC Evolutionary Biology, vol. 7, article 137, 2007.
[35]
B. Nevado, V. Fazalova, T. Backeljau, M. Hanssens, and E. Verheyen, “Repeated unidirectional introgression of nuclear and mitochondrial dna between four congeneric Tanganyikan cichlids,” Molecular Biology and Evolution, vol. 28, no. 8, pp. 2253–2267, 2011.
[36]
C. Sturmbauer, W. Salzburger, N. Duftner, R. Schelly, and S. Koblmüller, “Evolutionary history of the Lake Tanganyika cichlid tribe Lamprologini (Teleostei: Perciformes) derived from mitochondrial and nuclear DNA data,” Molecular Phylogenetics and Evolution, vol. 57, no. 1, pp. 266–284, 2010.
[37]
S. Koblmüller, N. Duftner, K. M. Sefc et al., “Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika—the result of repeated introgressive hybridization,” BMC Evolutionary Biology, vol. 7, article 7, 2007.
[38]
R. Schelly, W. Salzburger, S. Koblmüller, N. Duftner, and C. Sturmbauer, “Phylogenetic relationships of the lamprologine cichlid genus Lepidiolamprologus (Teleostei: Perciformes) based on mitochondrial and nuclear sequences, suggesting introgressive hybridization,” Molecular Phylogenetics and Evolution, vol. 38, no. 2, pp. 426–438, 2006.
[39]
S. Koblmüller, B. Egger, C. Sturmbauer, and K. M. Sefc, “Evolutionary history of Lake Tanganyika's scale-eating cichlid fishes,” Molecular Phylogenetics and Evolution, vol. 44, no. 3, pp. 1295–1305, 2007.
[40]
S. Koblmüller, B. Egger, C. Sturmbauer, and K. M. Sefc, “Rapid radiation, ancient incomplete lineage sorting and ancient hybridization in the endemic Lake Tanganyika cichlid tribe Tropheini,” Molecular Phylogenetics and Evolution, vol. 55, no. 1, pp. 318–334, 2010.
[41]
B. Nevado, S. Koblmüller, C. Sturmbauer, J. Snoeks, J. Usano-Alemany, and E. Verheyen, “Complete mitochondrial DNA replacement in a Lake Tanganyika cichlid fish,” Molecular Ecology, vol. 18, no. 20, pp. 4240–4255, 2009.
[42]
T. Takahashi and S. Koblmüller, “The adaptive radiation of cichlid fish in Lake Tanganyika: a morphological perspective,” International Journal of Evolutionary Biology, vol. 2011, Article ID 620754, 14 pages, 2011.
[43]
G. W. Coulter, Lake Tanganyika and Its Life, Oxford University Press, London, UK, 1991.
[44]
G. Fryer, “Evolution in ancient lakes: radiation of Tanganyikan atyid prawns and speciation of pelagic cichlid fishes in Lake Malawi,” Hydrobiologia, vol. 568, no. 1, pp. 131–142, 2006.
[45]
N. Duftner, S. Koblmüller, and C. Sturmbauer, “Evolutionary relationships of the Limnochromini, a tribe of benthic deepwater cichlid fish endemic to Lake Tanganyika, East Africa,” Journal of Molecular Evolution, vol. 60, no. 3, pp. 277–289, 2005.
[46]
S. Koblmüller, N. Duftner, C. Katongo, H. Phiri, and C. Sturmbauer, “Ancient divergence in bathypelagic Lake Tanganyika deepwater cichlids: mitochondrial phylogeny of the tribe Bathybatini,” Journal of Molecular Evolution, vol. 60, no. 3, pp. 297–314, 2005.
[47]
D. H. Eccles, “Is speciation of demersal fishes in Lake Tanganyika restrained by physical limnological conditions?” Biological Journal of the Linnean Society, vol. 29, no. 2, pp. 115–122, 1986.
[48]
U. K. Schliewen and B. Klee, “Reticulate sympatric speciation in Cameroonian crater lake cichlids,” Frontiers in Zoology, vol. 1, article 5, 2004.
[49]
J. P. Sullivan, S. Lavoué, M. E. Arnegard, and C. D. Hopkins, “AFLPs resolve phylogeny and reveal mitochondrial introgression within a species flock of African electric fish (Mormyroidea: Teleostei),” Evolution, vol. 58, no. 4, pp. 825–841, 2004.
[50]
F. Herder, A. W. Nolte, J. Pfaender, J. Schwarzer, R. K. Hadiaty, and U. K. Schliewen, “Adaptive radiation and hybridization in Wallace's Dreamponds: evidence from sailfin silversides in the Malili Lakes of Sulawesi,” Proceedings of the Royal Society B, vol. 273, no. 1598, pp. 2209–2217, 2006.
[51]
R. Takahashi, K. Watanabe, M. Nishida, and M. Hori, “Evolution of feeding specialization in Tanganyikan scale-eating cichlids: a molecular phylogenetic approach,” BMC Evolutionary Biology, vol. 7, no. 1, article 195, 2007.
[52]
P. A. Larsen, M. R. Marchán-Rivadeneira, and R. J. Baker, “Natural hybridization generates mammalian lineage with species characteristics,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 25, pp. 11447–11452, 2010.
[53]
V. Sternkopf, D. Liebers-Helbig, M. S. Ritz, J. Zhang, A. J. Helbig, and P. de Knijff, “Introgressive hybridization and the evolutionary history of the herring gull complex revealed by mitochondrial and nuclear DNA,” BMC Evolutionary Biology, vol. 10, no. 1, article 348, 2010.
[54]
D. A. Joyce, D. H. Lunt, M. J. Genner, G. F. Turner, R. Bills, and O. Seehausen, “Repeated colonization and hybridization in Lake Malawi cichlids,” Current Biology, vol. 21, no. 3, pp. R108–R109, 2011.
[55]
M. Poll, “Classification des Cichlidae du lac Tanganika. Tribus, genres et espèces,” Academie Royale de Belgique, Mémoires de la Classe des Sciences, vol. 45, pp. 1–163, 1986.
[56]
M. L. J. Stiassny, “Phylogenetic versus convergent relationship between piscivorous cichlid fishes from Lakes Malawi and Tanganyika,” Bulletin of the British Museum of Natural History, vol. 40, pp. 67–101, 1981.
[57]
M. Nishida, “Phylogenetic relationships and evolution of Tanganyikan cichlids: a molecular perspective,” in Fish Communities in Lake Tanganyika, H. Kawanabe, M. Hori, and M. Nagoshi, Eds., pp. 1–23, Kyoto University Press, Kyoto, Japan, 1997.
[58]
E. Lippitsch, “Phylogenetic study of cichlid fishes in Lake Tanganyika: a lepidological approach,” Journal of Fish Biology, vol. 53, no. 4, pp. 752–766, 1998.
[59]
T. Takahashi, “Systematics of Tanganyikan cichlid fishes (Teleostei: Perciformes),” Ichthyological Research, vol. 50, no. 4, pp. 367–382, 2003.
[60]
A. Konings, Tanganyika Cichlids in Their Natural Habitat, Cichlid Press, El Paso, Tex, USA, 1998.
[61]
M. J. Genner, P. Nichols, G. R. Carvalho, R. L. Robinson, P. W. Shaw, and G. F. Turner, “Reproductive isolation among deep-water cichlid fishes of Lake Malawi differing in monochromatic male breeding dress,” Molecular Ecology, vol. 16, no. 3, pp. 651–662, 2007.
[62]
S. Koblmüller, W. Salzburger, and C. Sturmbauer, “Evolutionary relationships in the sand dwelling cichlid lineage of Lake Tanganyika suggest multiple colonization of rocky habitats and convergent origin of biparental mouthbrooding,” Journal of Molecular Evolution, vol. 58, no. 1, pp. 79–96, 2004.
[63]
S. A. Miller, D. D. Dykes, and H. F. Polesky, “A simple salting out procedure for extracting DNA from human nucleated cells,” Nucleic Acids Research, vol. 16, no. 3, p. 1215, 1988.
[64]
R. Whitlock, H. Hipperson, M. Mannarelli, R. K. Butlin, and T. Burke, “An objective, rapid and reproducible method for scoring AFLP peak-height data that minimizes genotyping error,” Molecular Ecology Resources, vol. 8, no. 4, pp. 725–735, 2008.
[65]
M. Nei and W. H. Li, “Mathematical model for studying genetic variation in terms of restriction endonucleases,” Proceedings of the National Academy of Sciences of the United States of America, vol. 76, no. 10, pp. 5269–5273, 1979.
[66]
D. L. Swofford, PAUP*: Phylogenetic Analysis Using Parsimony (and Other Methods), version 4.0b2a, Sinauer, Sunderland, Mass, USA, 2000.
[67]
R. Luo, A. L. Hipp, and B. Larget, “A Bayesian model of AFLP marker evolution and phylogenetic inference,” Statistical Applications in Genetics and Molecular Biology, vol. 6, no. 1, pp. 1–30, 2007.
[68]
W. J. M. Koopman, V. Wissemann, K. de Cock et al., “AFLP markers as a tool to reconstruct complex relationships: a case study in Rosa (Rosaceae),” American Journal of Botany, vol. 95, no. 3, pp. 353–366, 2008.
[69]
J. P. Huelsenbeck and F. Ronquist, “MRBAYES: Bayesian inference of phylogenetic trees,” Bioinformatics, vol. 17, no. 8, pp. 754–755, 2001.
[70]
F. Ronquist, J. P. Huelsenbeck, and P. van der Mark, MrBayes 3.1. Manual Draft 5/26.2005, School of Computational Science, Florida State University, Tallahassee, Fla, USA, 2005.
[71]
A. Rambaut and A. J. Drummond, “Tracer v1.5,” 2009, http://tree.bio.ed.ac.uk/software/tracer/.
[72]
K. Takahashi, Y. Terai, M. Nishida, and N. Okada, “Phylogenetic relationships and ancient incomplete lineage sorting among cichlid fishes in lake Tanganyika as revealed by analysis of the insertion of retroposons,” Molecular Biology and Evolution, vol. 18, no. 11, pp. 2057–2066, 2001.
[73]
K. G. McCracken and M. D. Sorenson, “Is homoplasy or lineage sorting the source of incongruent mtDNA and nuclear gene trees in the stiff-tailed ducks (Nomonyx-Oxyura)?” Systematic Biology, vol. 54, no. 1, pp. 35–55, 2005.
[74]
O. Seehausen, “Hybridization and adaptive radiation,” Trends in Ecology and Evolution, vol. 19, no. 4, pp. 198–207, 2004.
[75]
H. Shimodaira and M. Hasegawa, “Multiple comparisons of log-likelihoods with applications to phylogenetic inference,” Molecular Biology and Evolution, vol. 16, no. 8, pp. 1114–1116, 1999.
[76]
R. E. Kass and A. E. Raftery, “Bayes factors,” Journal of the American Statistical Association, vol. 90, no. 430, pp. 773–795, 1995.
[77]
M. A. Newton and A. E. Raftery, “Approximate Bayesian inference by weighted likelihood bootstrap,” Journal of the Royal Statistical Society Series B, vol. 56, no. 1, pp. 3–48, 1994.
[78]
M. A. Suchard, R. E. Weiss, and J. S. Sinsheimer, “Bayesian selection of continuous-time Markov chain evolutionary models,” Molecular Biology and Evolution, vol. 18, no. 6, pp. 1001–1013, 2001.
[79]
D. M. Althoff, M. A. Gitzendanner, and K. A. Segraves, “The utility of amplified fragment length polymorphisms in phylogenetics: a comparison of homology within and between genomes.,” Systematic Biology, vol. 56, no. 3, pp. 477–484, 2007.
[80]
B. R. Holland, A. C. Clarke, and H. M. Meudt, “Optimizing automated AFLP scoring parameters to improve phylogenetic resolution,” Systematic Biology, vol. 57, no. 3, pp. 347–366, 2008.
[81]
K. L. Shaw, “Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 25, pp. 16122–16127, 2002.
[82]
C. A. Machado and J. Hey, “The causes of phylogenetic conflict in a classic Drosophila species group,” Proceedings of the Royal Society B, vol. 270, no. 1520, pp. 1193–1202, 2003.
[83]
A. Willyard, R. Cronn, and A. Liston, “Reticulate evolution and incomplete lineage sorting among the ponderosa pines,” Molecular Phylogenetics and Evolution, vol. 52, no. 2, pp. 498–511, 2009.
[84]
L. L. Knowles, “The burgeoning field of statistical phylogeography,” Journal of Evolutionary Biology, vol. 17, no. 1, pp. 1–10, 2004.
[85]
P. R. Grant and B. R. Grant, “Hybridization of bird species,” Science, vol. 256, no. 5054, pp. 193–197, 1992.
[86]
T. Hatfield and D. Schluter, “Ecological speciation in sticklebacks: environment-dependent hybrid fitness,” Evolution, vol. 53, no. 3, pp. 866–873, 1999.
[87]
D. Schluter, “Ecology and the origin of species,” Trends in Ecology and Evolution, vol. 16, no. 7, pp. 372–380, 2001.
[88]
M. N. Verzijden, J. van Heusden, N. Bouton, F. Witte, C. Ten Cate, and H. Slabbekoorn, “Sounds of male Lake Victoria cichlids vary within and between species and affect female mate preferences,” Behavioral Ecology, vol. 21, no. 3, pp. 548–555, 2010.
[89]
M. Plenderleith, C. van Oosterhout, R. L. Robinson, and G. F. Turner, “Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish,” Biology Letters, vol. 1, no. 4, pp. 411–414, 2005.
[90]
M. R. Kidd, N. Duftner, S. Koblmüller, C. Sturmbauer, and H. Hofmann, “Repeated parallel evolution of parental care strategies within Xenotilapia, a genus of cichlid fishes from Lake Tanganyika,” PLoS ONE, vol. 7, no. 2, Article ID e31236, 2012.
