Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes

Abstract

The polychromatic and trophically polymorphic Midas cichlid fish species complex (Amphilophus cf. citrinellus) is an excellent model system for studying the mechanisms of speciation and patterns of phenotypic diversification in allopatry and in sympatry. Here, we first review research to date on the species complex and the geological history of its habitat. We analyse body shape variation from all currently described species in the complex, sampled from six crater lakes (maximally 1.2-23.9 kyr old) and both great lakes in Nicaragua. We find that Midas cichlid populations in each lake have their own characteristic body shape. In lakes with multiple sympatric species of Midas cichlid, each species has a distinct body shape. Across the species complex, most body shape change relates to body depth, head, snout and mouth shape and caudal peduncle length. There is independent parallel evolution of an elongate limnetic species in at least two crater lakes. Mitochondrial genetic diversity is higher in crater lakes with multiple species. Midas cichlid species richness increases with the size and age of the crater lakes, though no such relationship exists for the other syntopic fishes. We suggest that crater lake Midas cichlids follow the predicted pattern of an adaptive radiation, with early divergence of each crater lake colonization, followed by intralacustrine diversification and speciation by ecological adaptation and sexual selection.

Figure 1.

The crater lakes of Nicaragua lie in the craters of dormant volcanoes along the fault lines that run along the western coast. Lakes discussed in the text are noted. 1. Miraflores, 2. San Antonio, 3. Tipitapa, 4. Las Isletas, As. = Asososca. Scale bar = 20 km.

Figure 2.

Location of 15 homologous landmarks used for geometric morphometrics to describe body shape.

Figure 3.

Plot of all specimens derived from a CVA. Each lake is shown in a different colour. Each dot represents the multivariate morphospace of a different specimen in CV1 and CV2. As. = Asososca.

Figure 4.

Shape change associated with CV1 across the species complex from the analysis of all eight lakes combined. The circle represents an average consensus body shape for all Midas cichlids. The bar terminus represents the shift in body shape that is associated with the first CV. The distortion in the grid shows the local shape change associated with the difference between the consensus shape and the shape change described in CV1. Thus, the primary change in body shape across all Midas cichlids relates to body elongation and mid-body height. Scale factor = 10.

Figure 5.

(a) There is a complete morphospace difference between A. citrinellus from each of the two lakes, which is primarily described by CV2. Conversely, most of the variation between the two A. labiatus populations and between species is described along CV1. All interspecific and population comparisons are significantly different in body shape (p < 0.001) Each dot represents the multivariate morphospace of an individual specimen. (b) The shape changes between the average (i.e. consensus) shape of A. citrinellus (black dot) and A. labiatus (line terminus) in great lakes Managua and Nicaragua. In both lakes, both species are completely differentiated by a DFA. No scale factor applied.

Figure 6.

(a) The first two axes of the CVA can distinguish all four species within crater Lake Apoyo. Each dot represents the multivariate morphospace of an individual specimen. (b) Body shape variation for each of the four species in Apoyo compared with a consensus body shape. The line terminus indicates the average local shape change in the species of interest, compared with a consensus average shape for all four species of Midas cichlid that are endemic to Lake Apoyo (black dot). Scale factor = 7.5.

Figure 7.

(a) The first two axes of the CVA can distinguish all three species within crater Lake Xiloá. Each dot represents the multivariate morphospace of an individual specimen. (b) Body shape variation for each of the three described species of Xiloá compared with the consensus body shape of all three species of the lake. The line terminus indicates the average local shape change in the species of interest, compared with a consensus average shape (black dot). Scale factor = 7.5.

Figure 8.

The morphospaces of individual specimens in the limnetic species, A. zaliosus (endemic to Lake Apoyo) and A. sagittae (endemic to Lake Xiloá) are explained by the same direction of principal components (primarily along PC1). Benthic species are better distinguished along PC2.

Figure 9.

There is a negative trend between PD, which describes the amount of body shape variation within each crater lake, and rarefied allelic richness. A line of best fit is drawn in grey. Each crater lake is noted, with the number in parentheses indicating the number of currently described Midas cichlid species in the lake.

Figure 10.

Midas cichlid species richness increases significantly with crater lake age (in thousands of years; grey dots and grey line of best fit) and surface area (in km²; black dots and black line of best fit). Some crater lakes will increase in species richness (along x-axis) if more species are formally described in the future. The same relationship does not hold for other fish species in the crater lakes.