Testing Conjectures About Morphological Diversity in Cichlids of Lakes Malawi and Tanganyika

Copeia, 2005(2), pp. 359±373 Testing Conjectures about Morphological Diversity in Cichlids of Lakes Malawi and Tanganyika PROSANTA CHAKRABARTY The morphological diversity of Malawi and Tanganyika cichlids has often been qualitatively described, but rarely have hypotheses based on these descriptions been tested empirically. Using landmark based geometric morphometrics, shapes are an- alyzed independent of other aspects of the body form (e.g., size). The estimation of shape disparity, the quantitative measure of the variance of these raw shapes, can then be applied in order to objectively test hypotheses about morphological diversity. The shape disparity within and between different groups is explored as well as how it is partitioned within the cichlid body. Tanganyika cichlids are found to have signi®cantly greater shape disparity than Malawi cichlids. Ectodini is found to have signi®cantly greater shape disparity than other Great Lake tribes. Piscivorous cichlids are signi®cantly more disparate in shape than cichlids with other diets, and the shape disparity of the cranial region was signi®cantly greater than that of the post- cranial region. ``We begin by describing the shape of an object in Lake cichlids have been described (Bouton et the simple words of common speech: we end by al., 2002a; Wautier et al., 2002; Kassam et al., de®ning it in the precise language of mathemat- 2003a) including evidence of convergence of ics; and the one method tends to follow the other these elements between lakes (RuÈber and Ad- in strict scienti®c order and historical continui- ams, 2001; Kassam et al., 2003b); however, those ty.''±D'Arcy Thompson, 1917 (On Growth studies dealt only with patterns of morphologi- and Form) cal diversity rather than with its magnitude. A broad analysis of the morphological diversity of HE cichlids of the Great Lakes of East Af- Great Lakes cichlids has yet to be done despite T rica are favorite textbook examples of sev- its relevance. The analyses presented here at- eral notable elements of natural history and tempt to objectively explore the morphological evolutionary theory, including: shape and diet diversity of a large and taxonomically diverse convergence, sympatric and allopatric specia- sampling (ø 100 spp.) of Great Lake cichlids. tion, adaptive radiations, species ¯ocks, and The Great Lakes of East Africa, comprised of Fisherian runaway sexual selection (Carroll, Lakes Tanganyika, Malawi, and Victoria, each 1997; Futuyma, 1998; Strickberger, 2000). The have a cichlid fauna of several hundred de- foundations for some of these ideas are the sub- scribed endemic species; however, the ®nal in- jective impressions of workers about the mor- ventory will most probably exceed a total of phological diversity of these cichlids. Such in- 1,000 species (Kullander, 1998; Korn®eld and ferences are not empirically repeatable or quan- Smith, 2000). Lake Victoria has recently under- ti®able. Likewise, disagreements over the mag- gone a signi®cant loss of its cichlids due to a nitude of morphological diversity in different number of anthropogenic factors (Meyer, 1993; groups are left unresolved. This study tests con- Seehausen et al., 1997; Stiassny and Meyer, jectures about morphological diversity from an 1999) and is not studied here. estimation of the total variance among shapes Lakes Malawi and Tanganyika, the focal (i.e., shape disparity, de®ned mathematically in points of this study, are among the ten largest Materials and Methods). lakes in the world by area and depth and con- Contrasting levels of morphological diversity tain more ®sh species than any other lakes (Fry- has been dif®cult because of a lack of metrics er and Iles, 1972). These two lakes hold the ma- that can be compared statistically. Recently a va- jority of cichlid species diversity; cichlids are riety of metrics have been devised for quantify- also found in other parts of Africa, the Middle ing morphological diversity (5 morphological East, the Neotropics, Madagascar, and the In- disparity; Foote, 1993; Fortey et al., 1996; Eble, dian sub-continent (Kullander, 1998; Murray, 2000), including those suited to the analyses of 2001). Lake Tanganyika has been recognized as geometric shape (Zelditch et al., 2003, 2004). a harbor for the lineages that gave rise to the Correlation in external geometric shape and cichlids of Malawi and Victoria (Nishida, 1991; trophic morphology of small groups of Great Meyer et al., 1994). Both Lake Tanganyika and q 2005 by the American Society of Ichthyologists and Herpetologists 360 COPEIA, 2005, NO. 2 the cichlid lineages it contains are recognized trophic levels and habitats occupied by mem- as several million years older than Lake Malawi bers of those clades. Lamprologini and Ectodini and its cichlids (Meyer, 1993). The many hun- have both been proposed as occupying the dreds of cichlid species these lakes contain are greatest amount of morphological, trophic, and proposed to have evolved over the course of less habitat diversity of any Great Lake tribes than ®ve million years (Meyer, 1993). (Sturmbauer and Meyer, 1993; Stiassny, 1997; Testing hypotheses about broader mecha- Barlow, 2000). It is predicted that these two nisms associated with the rapid speciation of tribes will be more disparate than other groups. these cichlids is beyond the scope of this paper. Piscivorous cichlids have less morphological However, measuring the magnitude of morpho- diversity than cichlids with other diets (Conjec- logical diversity that is the basis of those hypoth- ture 3). Piscivorous cichlids are often demon- eses is a necessary ®rst step. Four conjectures strated as having similar morphologies and/or are composed to re¯ect general observations convergent shapes (Kocher et al., 1993; Meyer, that have been made about Great Lake cichlid 1993; Martin and Bermingham, 1998). It has morphological diversity. These are listed below been proposed that this constraint may be due and abbreviated as C1±C4 for the remainder of to the relatively minor morphological modi®- this paper. cations necessary for variation in this diet class Morphological diversity of Lake Tanganyika (Greenwood, 1974; Liem, 1978; Stiassny, 1981). cichlids is greater than that of Lake Malawi cich- As Fryer and Iles (1972) noted, ``In general, the lids (Conjecture 1). Several mechanisms have piscivorous cichlids exhibit the adaptations been proposed to explain the observation that common to many piscivorous ®shes±stream- the cichlids of Lake Tanganyika have greater lined, and not infrequently slender bod- morphological diversity than Malawi cichlids, ies. large eyes; mouths with a very wide gape.'' despite having half to a third of the species rich- One would thus expect the piscivorous cichlids ness of Lake Malawi (Greenwood, 1984a; Meyer, to have low shape diversity relative to cichlids in 1993; Salzburger et al., 2002). Included among other diet classes because of these commonly these is the notion that natural selection has shared features. This is because the conver- had suf®cient time to remove intermediate gence to the same or similar form reduced the morphologies only from Lake Tanganyika (2±4 amount of variance in shape of the group. million years old) and not Malawi (1±2 million The majority of differences between the years old; Greenwood, 1984a; Mayr, 1984; Mey- shapes of cichlids lie within the shape of the er, 1993). Other possibilities raised are that the head region (Conjecture 4). Several authors greater abundance of disjunct rocky habitats in have hypothesized that most of the differences Malawi allowed for higher occurrences of mi- between haplochromine cichlid species lie in cro-allopatric speciation (Fryer and Iles, 1972; the head (Greenwood, 1974, 1984b; Barel, Genner et al., 1999) or that sexual selection has 1983). Studies that correlate head shape with occurred without much corresponding mor- environmental variables or trophic level, with- phological change in Lake Malawi while other out considering the rest of the body, exemplify processes have occurred in Lake Tanganyika the acceptance of this assumption (Strauss, (Meyer, 1993; Parker and Korn®eld, 1997; Al- 1984; Bouton et al., 2002a and references with- bertson et al., 1999). Some have even proposed in). Conjecture 4 was tested for all the cichlid that the noted difference in morphological di- species sampled here from Lake Malawi and versity is due to the artifact of Tanganyika being Lake Tanganyika. Greenwood (1991) suggested better studied than Malawi (Kassam et al., that the trophic plasticity provided by the dual 2003b). Until now, the foundational assumption oral and pharyngeal-feeding systems of cichlids of these hypotheses±whether there is in fact a might explain much of the corresponding mor- difference in the morphological diversity be- phological diversity of the group. Potentially, tween lakes±has never been tested. those modi®cations of the cranial elements, re- Lamprologini or Ectodini have the greatest ¯ected externally, explain more of the shape di- morphological diversity of the Great Lake tribes versity than do post-cranial modi®cations. (Conjecture 2). Morphological diversity of All four of these conjectures predict a pattern Great Lake cichlid clades has been a subject of other than the default explanation that mor- debate (Sturmbauer and Meyer, 1993; Stiassny, phological diversity increases with the number 1997; Barlow, 2000), particularly with respect to of species sampled. Others have shown persua- the 12 tribes into which these cichlids have been sively that

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