;;;;;;;;;;;;;;;;;;;;;; anthropogenic threats, undoubtedly taking their Beak of the Fish: What fascinating and irreplaceable stories about evolution with them. Cichlid Flocks Reveal East African Great Lakes and Their Cichlid Flocks About Speciation Like Darwins finches that were isolated on islands, flocks of cichlid fishes have also undergone Processes adaptive radiations within insular habitats: the Great Lakes of East Africa. These tropical lakes are among by Holly Jessop the largest lakes in the world, reaching depths of 1500-m and areas of about 69,000-km2. Fortuitously, Introduction differences in geologic origins, features, and ages ������������������������������������������������������������������������������������������ are useful when studying the evolution of endemic influenced Charles Darwins formative ideas on cichlid fishes. Of the three lakes, Lake Tanganyika natural selection and its connections with speciation. is the oldest (forming 9-12 million years ago) and Today, the adaptive radiation evident in the beaks of deepest. This lake of 34,000-km2 hosts twelve flocks those fourteen different species of birds continues to of cichlids that have radiated into about 250 species. provide the classic textbook example of evolution in The other deep rift lake, Lake Malawi, is about the action. However, if the creation of a mere fourteen same size but is younger (formed 1-2 million years different species has been instructive, then an ago). This intermediate lake hosts about a thousand explosive creation of well over a thousand should species that have all radiated from just one flock reveal a great deal more about speciation processes. ancestor. The youngest (750,000 years old), largest, The fish family Cichlidae provides such a case: these and most shallow, Lake Victoria hosts about 500 fish have evolved thousands of new species within species that have also emanated from one cichlid their insular lake homes, and furthermore have flock. (Barlow 2000; Salzburger et al. 2005). Since the done so on extremely rapid time scales. Indeed, their greater depths of the lakes lack oxygen, cichlids are explosive and rapid cladogenesis has made cichlids confined to the surface layers and shallow benthic the greatest extant vertebrate radiation known. The habitats of the lakes. These habitats are characterized young evolutionary age of cichlids also provides a by sandy bottoms punctuated with patches of rocky window into the earliest stages of diversification, such outcroppings. (Barlow 2000). that speciation may be studied as an ongoing process of change. Moreover, the recent multitude of species Cichlid Species: A Kaleidoscope of Form and Color within the cichlid family provides an opportunity to The species composing the cichlid flocks of look for patterns in speciation processes. Such studies these East African Great Lakes possess a bounty of have suggested a three-stage pattern underlying variation in both form and color. Indeed, these fish speciation that may be generally applicable to the are prized for their beauty and interesting diversity, evolutionary origins of many other vertebrate species and as such, are popular with aquarium hobbyists. Danley & Kocher 2001; Streelman & Danley 2003). The visual scenes within the lakes are themselves Of special interest is the stage of evolution in which reminiscent of aquaria with swarms of colorful fish in different feeding structures arise among these fishes, a myriad of hues and shapes. With this abundance of particularly since parallels exist between the beaks similar fish fauna, species and their phylogenies have of Darwins finches and the jaws of cichlids. Modern been difficult to determine, using only morphology genetic techniques are responsible for insight into and color characteristics; are similarly shaped but this three-step pattern, and are increasingly being differently colored fish morphs of the same or used to further uncover the detail in the processes different species? Behavioral differences in feeding responsible for the remarkable diversity of cichlids. strategies and reproduction often clarified these Unfortunately, even as cichlids are just beginning determinations: fish that looked similar but fed, to provide the post-Darwinian age with highly mated, or reared young differently were considered valuable insights into the mechanisms of evolutionary separate species (Genner & Turner 2005). However, change, these fish are being rapidly destroyed by modern molecular techniques that examine genetic 16 characteristics have recently provided an additional Not only did cichlids in the Great Lakes means by which cichlid diversification can be explosively and rapidly diversify, they also separately ���������������������������������������������������������������������������������������������������������� converged into very similar morphologies. Figure 2 For example, Meyer et al. (1990) found no overlaps illustrates several cichlids from Lakes Tanganyika in the mitochondrial DNA types of 14 cichlid species and Malawi that share similar body forms and engage from Lake Victoria; they concluded that these fish in parallel lifestyles. Studies prior to Meyer et al. were not merely alternative morphs of one species. 1990) argued that such cichlids were polyphyletic: That is, their classification as separate species was these outwardly similar fish from different lakes justifiable given their unique genetic characters. Now, were derived from different ancestral lines, and in cichlid species are regularly defined using genetic turn were most closely related to each other. Instead, characters, in addition to information on morphology, the advent of molecular phylogenetic studies have color, and behavioral traits (Turner et al. 2001; Genner repeatedly shown that these cichlid radiations have Turner 2005). occurred separately, each within their own lake basin Meyer et al. 1990, Kocher et al. 1993, Meyer 1993, Origins: Out of Lake Tanganyika Comes Explosive, Nagl et al. 2000, Verheyan et al. 2003, Salzburger et Rapid, and Parallel Evolution al. 2005). For example, the uniquely fleshy lips of the Remarkably, nearly all of the cichlid species in Placidochromis fishes of Lake Malawi arose separately the East African Great Lakes are endemic. Moreover, from the fleshy lips of the Lobochilotes cichlids of Lake none of these cichlid species are shared between Tanganyika; Placidochromis are more closely related the lakes despite belonging to the same family to their own proximate Lake Malawi flocks than to Salzburger et al. 2005). Since they share numerous their albeit morphologically similar cousins of Lake similarities, an understanding of how these fish are Tanganyika. Even within the same lake, these fish inter-related becomes an important initial step in seem to separately evolve similar morphologies. untangling the mystery of how many differences For example, Ruber et al. (1999) found that some evolved. Again, modern genetic techniques have cichlids of Lake Tanganyika that share the same proven to be the most useful tool for this detective dentition patterns are not monophyletic. That is, work: the first examination of mitochondrial DNA different species separately evolved the same tooth of cichlids from the Great Lakes by Meyer et al. shape. Similarly, Allender et al. (2003) examined the 1990) revealed that the cichlids of each lake are genetic differences between like-colored fish from monophyletic. The family tree that emerges from the northern and southern portions of Lake Malawi. this investigation also reveals that Lake Tanganyika Using over 2000 genetic loci, they built phylogenies cichlids are the ancestors from which the cichlids in demonstrating that the same color patterns had the other two Great Lakes are derived (Figure 1). The independently evolved within different parts of finding that well over a thousand species of cichlids the lake. That is, the northern and southern fish are in Lakes Malawi and Victoria evolved from a single unrelated, but separately evolved the same color source reveals that speciation processes within these types via divergent selection. Thus, both between and lakes were remarkably explosive. within them, the Great Lakes have been reservoirs of Furthermore, Meyer et al. (1990) utilized a frequent parallel evolution (Genner & Turner 2005; molecular clock in their analysis of mitochondrial Kassam et al. 2006). DNA haplotypes, to estimate the ages of different cichlid lake flocks. They concluded that the Victorian Multistage Evolutionary Patterns cichlids are newcomers originating less than 200,000 The frequent occurrences of parallel evolution years ago, while the ages of the Lake Malawi and within cichlid flocks, added to their numerous and Tanganyika cichlids also match with the (relatively recent cladogenesis events, provide a highly useful young) geologic ages of those lakes. A recent case study of adaptive radiation. What can cichlids extensive study by Salzburger et al. (2005) that used reveal about speciation processes; are there common over twice the number of mitochondrial base pairs factors or underlying patterns? Once again, modern and ten times the number of species, confirms that phylogenetic techniques have been useful for these Lake Tanganyika is both the geographic and genetic evolutionary investigations. The 1990 mitochondrial origin for the cichlids of the other Great Lakes. This DNA sequencing study by Meyer et al. first found finding, that the multitude of species in the Great that the cichlids in Lake Malawi could be divided