Covariation of body shape and trophic morphology
In this study, we examined variation in body shape and trophic morphology in several genetic lineages of eretmodine cichlids from Lake Tanganyika. Using CVA, we found significant differences in body shape among populations (Fig. 3), and the resulting ordination plot revealed that populations with different tooth types were well separated, particularly along the first CV axis. Specimens with an Eretmodus-like dentition were at the positive extreme of this axis and those with a Tanganicodus-like dentition at the negative extreme (fishes with a Spathodus-like tooth shape were intermediate). Further, specimens with an Eretmodus-like tooth shape from the genetically distinct A and C lineages were also well separated in the CV plot, corroborating results from other studies that found differences in dentition (Huysseune et al., 1999) and feeding behaviour (Yamaoka, pers. comm.). We conclude that significant body shape variation exists in eretmodine cichlids, and that such variation seems to follow differences in oral tooth shape.
In addition to body shape, we quantified four trophic characters, and using multivariate regression and partial least squares analyses, we found that variation in trophic characters was significantly associated with variation in body shape. Specimens with low tooth counts and a small gape- and interorbital width had relatively elongated heads and a forward directed snout, while specimens with high tooth counts and a large gape- and interorbital width had deep heads and a ventrally directed snout. These results identify a significant body shape – trophic morphology relationship, which implies that characterization of eretmodine cichlids on the basis of body shape (Figs 3 & 4) also differentiates them for their suite of trophic characters (Fig. 5). Although this body shape – trophic character relationship is quite strong, what is not known is the potential cause of this association.
One obvious candidate that must be investigated is the influence of shared evolutionary history (phylogeny) on this body shape – trophic character association. We performed a PGLS analysis to account for covariation because of the phylogenetic relationships of the taxa. We found that the significant association of body shape and the trophic characters was still present even after the removal of phylogenetic signal from the data set. Therefore, some evolutionary mechanism other than phylogeny is required to explain the covariation between body shape and trophic characters in eretmodine cichlids.
Evolutionary causes of morphological change
The results presented here reveal that variation in eretmodine cichlid body shape corresponds more closely to trophic morphology than to the phylogenetic relationships revealed by mtDNA sequences. Thus, there appears to be conflicting patterns of phenetic similarity and phylogenetic relatedness in this cichlid tribe. Two possible evolutionary scenarios could explain this. The first is that particular body shapes, and suites of trophic characters, have multiple independent origins, and that convergent evolution and parallelism of both character sets are prevalent in this group. The alternative explanation is that the phylogenetic relationships proposed by the mtDNA sequences do not represent the true branching pattern among taxa, because of molecular introgression and population hybridization. Although we cannot completely rule out this second possibility, we find it to be quite improbable.
For introgression to explain the observed morphological pattern, many independent introgression events would be required. For instance, lineages A2 and C2 each have Tanganicodus dentition and body shapes, but are found within genetic lineages characterized by Eretmodus dentition and body shape (A and C lineages, respectively). Because they are geographically close to their sister clades, introgression is a possibility, but two independent introgression events would be required: one each for A2 and C2. There are other instances in the phylogeny however, where introgression is much less possible. For example, Spathodus and Tanganicodus are resolved in genetically clear distinct lineages (e.g. B and F; D and E, respectively). Because these populations do not have overlapping distributions, the opportunity for hybridization is nonexistent, and thus the possibility that introgression could occur and explain each of these instances is remote. Therefore, we feel that introgression is not a probable explanation of the observed pattern, and turn to some other evolutionary explanation.
Given that introgression is an improbable scenario, how can we explain the apparent convergent evolution of body shape and trophic morphology? We hypothesize that selection pressures imposed by similar ecological habitats has driven morphological evolution and trophic specialization multiple times, in independent lineages, in this group. Although this scenario requires a tight link between ecological specialization and habitat use, there is much support for this in eretmodine cichlids. Previous field studies have shown that E. cf. cyanostictus is specialized to feed on filamentous algae by scraping (Yamaoka et al., 1986; Sturmbauer et al., 1992; but see Liem, 1979). In contrast, T. irsacae with its acute dental arcade is an invertebrate picker (Yamaoka et al., 1986). The diet of S. erythrodon is intermediate and contains algae but also a high proportion of ostracods, copepods, and insect larvae (H. H. Büscher, pers. comm.).
The dentitional differences found by Yamaoka et al. (1986) and Huysseune et al. (1999), and our analysis on body shape variation among eretmodine cichlids, allow us to draw some tentative conclusions about the functional correlates of these characters in terms of their feeding ecology. The arrangement of tooth groups, the large number of oral teeth and gape width as well as the stout body shape characteristic of Eretmodus (Fig. 4) may be indicators of scraping abilities: more teeth and a broad jaw as found in Eretmodus imply an increase in scraping surface. The shape of the oral jaw teeth on the other hand may be important in prey grasping, broad equally sized uniscupid teeth with a flattened crown as seen in Eretmodus being more useful for scraping filamentous algae. On the other extreme of the ecomorphological axis, less densely spaced pointed uniscupid teeth as seen in Tanganicodus may be more useful for the capture of mobile prey by picking. Invertebrate picking in Tanganicodus may be further fascilitated by the small interorbital width increasing the ability to visually select food items and the fusiform body shape allowing faster manoeuvre.
A striking feature of the distribution of eretmodine cichlids is the occurrence of sympatric species pairs along most of the coastline that differ in tooth shape. However, in different parts of the lake, the members of these species pairs belong to different genetic lineages (e.g. Eretmodus lineage A sympatric with Tanganicodus lineage E, Eretmodus lineage C sympatric with Spathodus lineage F; Fig. 1, Table 1; Rüber et al., 1999). The highly significant relationship between tooth shape and body shape suggests parallel evolution of not only dental morphology, but also of body shape among genetically diverged lineages. The replicated evolution of morphologically divergent species pairs points to the presence of well defined trophic niches that have facilitated ecological segregation, and to the adaptive value of the observed morphological associations. It is probable that such covariation is produced by similar selective pressures on body shape and feeding morphology, rather than by developmental constraints, enabling the multiple independent invasions of the same adaptive zone.
Trophic resource partitioning and microhabitat segregation among sympatric eretmodine taxa has been indicated (Hori et al., 1983; Hori, 1987); but further ecological data are required to better understand the morphological divergence of these cichlids. Trophic segregation may be an important factor promoting divergence within and between populations (Schluter & McPhail, 1993; Robinson & Wilson, 1994; Schluter, 1996). Therefore, the adaptation to different trophic niches through the modification of trophic morphology, body shape, and feeding behaviour as found in the Eretmodini may account for the formation and maintenance of the high degree of diversity found in lacustrine cichlid communities (Galis & Metz, 1998; Bouton et al., 1999; Dieckmann & Doebeli, 1999). Our results seem to indicate that this ecological specialization and morphological divergence can occur rapidly, and independently of phylogeny even within a single cichlid tribe endemic to a single lake.