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Introduction
This book is a revised and greatly expanded version of the Malawi cichlids guide published in the Back to Nature Series in 1997. It contains several new chapters and the number of photos -- about 590 are new -- has doubled.
Since the publication of Charles R. Darwin's second most famous book ‘The Descent of Man’ in 1871 [1], sexual selection has been recognized as being important for speciation because it can mediate reproductive isolation [2], [3]. Darwin differentiated between two fundamental modes of sexual selection: (i) competition between members of the same sex (often males) for reproductive opportunity (‘intrasexual’), and (ii) active mate choice of members from one sex (often females) for certain members from the other sex (‘intersexual’). Particularly in the latter mode, mate choice is often based on visual ornaments, although color traits can serve with respect to both inter- and intrasexual communication and, hence, inter- and intrasexual selection [4], [5]. Moreover, there are instances where the role of ornaments was altered from a function in female choice to one in male-male competition or vice versa[6].
Color and pigmentation patterns seem to play a central role in the explosively radiating cichlid fish species in the East African Great Lakes in general, and in the haplochromine cichlids in particular [7], [8], [9], [10]. Haplochromines contain the vast majority of East African cichlid species with the entire species flocks of lakes Victoria (ca. 700 species) and Malawi (ca. 700 species), the tribe Tropheini from Lake Tanganyika (ca. 25 species) and most riverine East African cichlids (ca. 200 species) (see e.g. [11], [12]). Therefore haplochromines are not only the – by far – most species-rich tribe of cichlid fishes but also a model of radiating species. A prominent feature of the haplochromines is their wealth of color morphs and their sexual color dimorphism, which is what led many authors to postulate an important evolutionary role of sexual selection via female mate choice [13], [14], [15], [16]. Interestingly, all haplochromines are maternal mouthbrooders where females incubate the eggs in their buccal cavities (see e.g. [12], [17]). Mouthbrooding evolved from substrate spawning several times during cichlid evolution [18], but only the ‘modern haplochromines’ show a derived polygynous or polygynandrous maternal mouthbrooding system with males carrying egg-spots on their anal fins [12], [17], [19]. These ovoid markings consist of a transparent outer ring and a brightly colored yellow, orange or reddish center [17], [20], [21]. The conspicuous central area is formed by xanthophores – a pigment cell type containing carotenoids and pteridines [19], [22].
Egg-spots appear to be important in the courtship and spawning behavior of haplochromines [20], [21], [23], [24] (Figure 1C). The exact function of egg-spots is unknown, however, and several hypotheses exist that seek to explain their mode of action and their evolutionary origin.
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(A) A male of A. burtoni showing egg-spots on its anal fin. (B) Natural variation of egg-spots in A. burtoni. All these fish were caught and photographed at the south-eastern part of Lake Tanganyika in Zambia. (C) A typical courtship and mating cycle of a haplochromine starts with a lateral display of the male, to which the female responds; she then lays a clutch of eggs and immediately takes them up into her mouth. The male then presents the egg-spots on the anal fin; the female seemingly nuzzles at these egg-spots and the male releases sperm so that the eggs are fertilized within the females' mouth. The eggs and larvae then stay in the buccal cavity of the female for a period of several days to a few weeks. The arrow points to the location of an egg that the female is taking up into her mouth.
Wickler [20], [21] suggested that egg-spots on the male's anal fin mimic real eggs of a species and therefore function as signal (‘releaser’) during courtship and to maximize fertilization rates. The egg mimicry hypothesis is primarily based on the putatively similar appearance in shape and coloration of egg-spots and the eggs of the respective species [20], [21], [25]. However, egg-spots and eggs often do not match in size, shape and coloration, which is inconsistent with the mimicry hypothesis [26], [27]. Still, this mismatch between real and ‘dummy’ eggs may be due to a trade-off between attractiveness towards females and conspicuousness for predators [24]. Hert [23] was the first to experimentally test the egg-dummy scenario. She showed that in the species Astatotilapia elegans there were no differences in fertilization rates between males without and males with intact egg-spots, which at least partly contradicted the mimicry hypothesis. On the other hand, males with intact egg-spots fertilized twice as many clutches compared to males without egg-spots. Further mate choice trials revealed that females always chose males with egg-spots and preferred males with four egg-spots over males with one egg-spot. In Pseudotropheus aurora (now Maylandia aurora), females spawned more frequently with males displaying more egg-spots and male egg-spot number correlated significantly with the number of fertilized clutches [28]. Hert [23], [28] concluded that egg-spots serve as sexual advertisement and that disruptive selection on male egg-spots may have contributed to reproductive isolation and, hence, speciation. In mate choice trials with Pseudotropheus lombardoi (now Maylandia lombardoi), a Lake Malawi cichlid in which males display a single egg-spot, females preferred males with one egg-spot over males with an artificially added second one [29]. Couldridge [29] suggested that female preference maintains the single egg-spot in P. lombardoi and that egg-spots may be linked to species recognition.
Previous hypotheses regarding the function of egg-spots involve female choice as the main explanation for the maintenance of this conspicuous male trait (see above). Interestingly, however, essential sequences of courtship behavior like quivering and lateral display are also used in male-male interactions. When males fight, which happens frequently in territorial haplochromines, they quiver, move back and forward and attack sideways [30]. So, why shouldn't egg-spots play a role in male-male competition, too? There are several arguments that would implicate egg-spots with intrasexual selection. Importantly, egg-spots are, most likely, an honest signal of male quality, as carotenoids cannot be synthesized de novo by animals (pteridines, on the other hand, can be synthesized; yet, this process appears to also be costly) [31], [32]. There is evidence that dominant males often display more egg-spots [33], [34]. Moreover, competition among males appears as yet another important component of color evolution in cichlids [35], [36].
To understand the function of egg-spots in the haplochromine cichlid Astatotilapia burtoni, we conducted three experiments. First, females had a choice based on visual cues only between two size-matched males differing in egg-spot number (one trial with naturally varying numbers of egg-spots (experiment 1.1) and one trial with manipulated numbers of egg-spots (experiment 1.2)). Second, we performed a female four-way choice experiment in a partial partition set-up (see e.g. [16]), in which females had the choice between four size-matched males with manipulated egg-spot numbers; we measured fertilization rate and genotyped the offspring in order to assess female preference by determining paternity (experiment 2). Finally, we conducted male aggression trials to test for a potential role of egg-spots in male-male competition (experiment 3).
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