A sensory bias has triggered the evolution of egg-spots in cichlid fishes

Abstract

Although, generally, the origin of sex-limited traits remains elusive, the sensory exploitation hypothesis provides an explanation for the evolution of male sexual signals. Anal fin egg-spots are such a male sexual signal and a key characteristic of the most species-rich group of cichlid fishes, the haplochromines. Males of about 1500 mouth-brooding species utilize these conspicuous egg-dummies during courtship--apparently to attract females and to maximize fertilization success. Here we test the hypothesis that the evolution of haplochromine egg-spots was triggered by a pre-existing bias for eggs or egg-like coloration. To this end, we performed mate-choice experiments in the basal haplochromine Pseudocrenilabrus multicolor, which manifests the plesiomorphic character-state of an egg-spot-less anal fin. Experiments using computer-animated photographs of males indeed revealed that females prefer images of males with virtual ('in-silico') egg-spots over images showing unaltered males. In addition, we tested for color preferences (outside a mating context) in a phylogenetically representative set of East African cichlids. We uncovered a strong preference for yellow, orange or reddish spots in all haplochromines tested and, importantly, also in most other species representing more basal lines. This pre-existing female sensory bias points towards high-quality (carotenoids-enriched) food suggesting that it is adaptive.

Figure 1. Schematic consensus phylogeny of the East African cichlids based on mitochondrial and nuclear gene segments (after [1] , [25], [36]).

The haplochromines (indicated by grey branches) are a derived and species-rich clade. The males of most haplochromine species display anal fin egg-spots, just as exemplified here for Astatotilapia burtoni. A few ancestral species, such as Pseudocrenilabrus multicolor, do not have egg-spots. Note that A. burtoni belongs to a riverine clade and occurs within Lake Tanganyika and surrounding rivers.

Figure 2. Female preference tests in Pseudocrenilabrus multicolor using computer animated stimuli.

(A) The experimental set-up consists of an iMac computer behind an experimental aquarium (60×30×30 cm). Two animations are shown simultaneously (in this case a conspecific male and a heterospecific, Astatotilapia burtoni; see [B]). (B) Results from the ‘benchmark’ experiment, in which P. multicolor females were given the choice between a conspecific and a heterospecific (A. burtoni) male. The females reacted significantly more often with the animated image showing a conspecific male. (C) Results from the ‘red fringe’ experiments, in which P. multicolor were left the choice between a male with and one without the red fringe on the tip of the anal fin. We could not detect any difference in female response, which is also backed-up by two-way choice experiments with live fish (see Figure S1). (D) Results from the ‘egg-spot’ experiment, in which P. multicolor females could choose between a natural male and a male bearing an in- silico egg-spot. Females showed a significant preference for the male with the artificial egg-spot. Arrowheads indicate the minute differences between the images presented to the females.

Figure 3. Color preference tests in different East African cichlid species.

(A) Set-up of the field experiment at Lake Tanganyika. Fishes were presented five color dots on a transparent foil and we measured the number of pecks towards each dot. (B) Set-up of the laboratory experiments. Individual fishes were presented five color dots on a computer screen. (C) Ancestral character state reconstruction of color preferences in a phylogenetically representative set of cichlids from Lake Tanganyika. Most species clearly preferred orange or red colors. Importantly, also the substrate spawning lamprologines showed such a preference. (D–F) Results from the color-dot preference experiments in the laboratory with the haplochromines Astatotilapia burtoni (D) and Pseudocrenilabrus multicolor (E) and the lamprologine Julidochromis ornatus (F). Significant differences between males and females are indicated.