Incipient speciation driven by hypertrophied lips in Midas cichlid fishes?

Abstract

Sympatric speciation has been debated in evolutionary biology for decades. Although it has gained in acceptance recently, still only a handful of empirical examples are seen as valid (e.g. crater lake cichlids). In this study, we disentangle the role of hypertrophied lips in the repeated adaptive radiations of Nicaraguan crater lake cichlid fish. We assessed the role of disruptive selection and assortative mating during the early stages of divergence and found a functional trade-off in feeding behaviour between thick- and thin-lipped ecotypes, suggesting that this trait is a target of disruptive selection. Thick-lipped fish perform better on nonevasive prey at the cost of a poorer performance on evasive prey. Using enclosures in the wild, we found that thick-lipped fish perform significantly better in rocky than in sandy habitats. We found almost no mixed pairs during two breeding seasons and hence significant assortative mating. Genetic differentiation between ecotypes seems to be related to the time since colonization, being subtle in L. Masaya (1600 generations ago) and absent in the younger L. Apoyeque (<600 generations ago). Genome-wide differentiation between ecotypes was higher in the old source lakes than in the young crater lakes. Our results suggest that hypertrophied lips might be promoting incipient sympatric speciation through divergent selection (ecological divergence in feeding performance) and nonrandom mating (assortative mating) in the young Nicaraguan crater lakes. Nonetheless, further manipulative experiments are needed in order to confirm the role of hypertrophied lips as the main cue for assortative mating.

Rapid adaptation to a novel light environment: The importance of ontogeny and phenotypic plasticity in shaping the visual system of Nicaraguan Midas cichlid fish (Amphilophus citrinellus spp.)

“…Cichlid fishes are famous for their phenotypic diversity (e.g., Fryer & Iles, 1972;Meyer, 1993) and have been investigated also in terms of phenotypic plasticity. Some lineages more than others are phenotypically plastic in their ecologically crucial tooth morphology (Meyer, 1987;Schneider, Li, Meyer, & Gunter, 2014), but also hypertrophied lips, that play an essential role both in terms of natural and sexual selection (Machado-Schiaffino, Henning, & Meyer, 2014;Machado-Schiaffino et al, 2017). Besides, several other traits were shown to be particularly plastic in cichlids (reviewed in Schneider & Meyer, 2017).…”

quaddRAD: a new high‐multiplexing and PCR duplicate removal ddRAD protocol produces novel evolutionary insights in a nonradiating cichlid lineage

“…; Machado‐Schiaffino et al . ). Traits with potential adaptive values in the two lineages could have different underlying genetic bases that could alternatively hinder or promote their divergence even under similar selective regimes (Fruciano et al .…”

“…Disruptive selection, for example, could have been stronger in the A. citrinellus spp., thereby facilitating a faster divergence of adaptive traits accompanied by the occupation of the available ecological niches. Another possible explanation is that, even if disruptive selection promoted a first (weak) phenotypic divergence in the two lineages, A. centrarchus could not evolve strong assortative mating (that has been recently documented in Midas: Elmer et al 2009;Machado-Schiaffino et al 2017). Traits with potential adaptive values in the two lineages could have different underlying genetic bases that could alternatively hinder or promote their divergence even under similar selective regimes (Fruciano et al 2016a).…”

Genetic dissection of adaptive form and function in rapidly speciating cichlid fishes

“…; Burress ; Henning and Meyer ; Machado‐Schiaffino et al. ). Thick‐lipped ecomorphs are typically suction‐feeders that forage for prey within rocky crevices (Video S1) (Keenleyside ).…”

“…; Machado‐Schiaffino et al. ), generating sufficient suction power and detecting prey through sensorial specializations (Oliver and Arnegard ). Transcriptomic evidence has shown that hypertrophied lips in African and Neotropical cichlids share molecular‐developmental mechanisms (Colombo et al.…”