The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes

Abstract

The question of how genetic variation translates into organismal diversity has puzzled biologists for decades. Despite recent advances in evolutionary and developmental genetics, the mechanisms that underlie adaptation, diversification and evolutionary innovation remain largely unknown. The exceptionally diverse species flocks of cichlid fishes are textbook examples of adaptive radiation and explosive speciation and emerge as powerful model systems to study the genetic basis of animal diversification. East Africa's hundreds of endemic cichlid species are akin to a natural mutagenesis screen and differ greatly not only in ecologically relevant (hence naturally selected) characters such as mouth morphology and body shape, but also in sexually selected traits such as coloration. One of the most fascinating aspects of cichlid evolution is the frequent occurrence of evolutionary parallelisms, which has led to the question whether selection alone is sufficient to produce these parallel morphologies, or whether a developmental or genetic bias has influenced the direction of diversification. Here, I review fitness-relevant traits that could be responsible for the cichlids' evolutionary success and assess whether these were shaped by sexual or natural selection. I then focus on the interaction and the relative importance of sexual vs. natural selection in cichlid evolution. Finally, I discuss what is currently known about the genes underlying the morphogenesis of adaptively relevant traits and highlight the importance of the forthcoming cichlid genomes in the quest of the genetic basis of diversification in this group.Keywords: adaptive evolution, evo-devo, evolutionary genomics, explosive speciation, organismal diversification, parallel evolution And what is the molecular basis of adaptation, evolutionary innovation and diversification? A key to these and related questions is the comparative study of exceptionally diverse yet relatively young species assemblages that have radiated in geographically well-defined areas. This strategy is anything but novel and dates back to the dawn of evolutionary research, with the fringillid finches of the Galapagos archipelago being the primary and most prominent case. These 14 songbird species -commonly referred to as Darwin's finches in honour of their discoverer -make up the classic example of adaptive radiation, i.e. the rapid proliferation of an ecologically and morphologically differentiated species assemblage from a single ancestor as a consequence of adaptation to divergent environments (Simpson 1953;Schluter 2000 The actual number of cichlid species in East Africa's Great Lakes is undetermined and, at least in the cases of Victoria and Malawi, a matter of debate. About 250 cichlid species are known to occur in Lake Tanganyika. Higher estimates for Lake Malawi range around 700-800 species (Snoeks 2001;Turner et al. 2001), making its fauna the most species-rich species flock known. The situation is less clear for the cichlid assemblage of Lake Victoria for two reasons. ...

Molecular Characterization of Two Endothelin Pathways in East African Cichlid Fishes

“…No other vertebrate family consists of such a great number of species (at least 3,000 species worldwide), such a degree of phenotypic diversity and such a rapid diversification rate. Above all, the species flocks of cichlids in the East African Great Lakes show the greatest variation in morphology, coloration, ecology, behavior, and reproductive biology (Barlow 2000;Coulter 1991;Fryer and Iles 1972;Keenleyside 1991;Kocher 2004;Kornfield and Smith 2000;Salzburger 2009;Seehausen 2006). Furthermore, the cichlids' occurrence in various geographic regions (Africa, India, Sri Lanka, and Central and South America) and the independent (and repeated) colonization of multiple African lakes (e.g., lakes Malawi, Tanganyika, and Victoria) form the basis for some outstanding cases of parallel evolution within and between lakes and regions (Duftner et al 2007;Elmer et al 2010;Kocher et al 1993).…”

“…Even though other groups of teleost fishes are characterized by the presence of pharyngeal structures that aid the passage of food into the esophagus, cichlid fishes show the greatest diversity in pharyngeal jaw morphology resulting in the efficient manipulation of a great variety of food. Thus, the pharyngeal jaw apparatus is thought to play an important role in niche specialization and, hence, speciation in cichlids (Liem 1973;Muschick et al 2011;Salzburger 2009). …”

“…Sexual selection is the other major factor that is likely to have contributed to the cichlids' species-richness (see, e.g., Meyer 1993;Salzburger 2009;Seehausen et al 1997;Turner & Burrows 1995), as indicated by the occurrence of multiple color morphs and sexual color dimorphism. This is particularly obvious in the most species-rich group of cichlids, the haplochromines.…”

“…Neural crest cells originate in the neural folds, and migrate away from the neural tube to form a wide variety of cell types across the whole body including neuron cells, pigment cells, craniofacial bones, Schwann cells, and smooth muscle cells (Chung et al 2009;Slack 2001). The genetic and developmental basis of the neural crest-derived tissues and specifically those involved in evolutionary key innovations is, hence, of great importance for the study of cichlid evolution (Salzburger 2009). Within the last decade several studies have focused on the genetic basis of naturally and sexually selected traits in cichlids (reviewed in Salzburger 2009).…”

Preface: Advances in cichlid research: behavior, ecology, and evolutionary biology

“…An elaborate reproductive behavior and a highly developed pharyngeal jaw have long been recognized as important key factors for the cichlids' evolutionary success (Liem, 1973;Keenleyside, 1991). However, the picture is not simple as additional intrinsic factors like mouth morphology, body shape and size, coloration, color perception, sound and smell, and phenotypic plasticity, combined with ecological opportunity, appear equally important for driving diversification of cichlids (Salzburger, 2009;Takahashi & Koblmüller, 2011;Wagner et al, 2012;Maan & Sefc, 2013;Salzburger et al 2014). In the current special issue, Burress (2015) reviews major ecological patterns associated with the evolutionary history of cichlids and discusses factors promoting ecological diversification as well as the consequences of ecological diversification by comparing and contrasting Neotropical and Afrotropical lineages.…”