Drivers and dynamics of a massive adaptive radiation in cichlid fishes.

Adaptive radiation is the likely source of much of the ecological and morphological diversity of life1-4. How adaptive radiations proceed and what determines their extent remains unclear in most cases1,4. Here we report the in-depth examination of the spectacular adaptive radiation of cichlid fishes in Lake Tanganyika. On the basis of whole-genome phylogenetic analyses, multivariate morphological measurements of three ecologically relevant trait complexes (body shape, upper oral jaw morphology and lower pharyngeal jaw shape), scoring of pigmentation patterns and approximations of the ecology of nearly all of the approximately 240 cichlid species endemic to Lake Tanganyika, we show that the radiation occurred within the confines of the lake and that morphological diversification proceeded in consecutive trait-specific pulses of rapid morphospace expansion. We provide empirical support for two theoretical predictions of how adaptive radiations proceed, the 'early-burst' scenario1,5 (for body shape) and the stages model1,6,7 (for all traits investigated). Through the analysis of two genomes per species and by taking advantage of the uneven distribution of species in subclades of the radiation, we further show that species richness scales positively with per-individual heterozygosity, but is not correlated with transposable element content, number of gene duplications or genome-wide levels of selection in coding sequences.

QTL study reveals candidate genes underlying host resistance in a Red Queen model system.

Specific interactions of host and parasite genotypes can lead to balancing selection, maintaining genetic diversity within populations. In order to understand the drivers of such specific coevolution, it is necessary to identify the molecular underpinnings of these genotypic interactions. Here, we investigate the genetic basis of resistance in the crustacean host, Daphnia magna, to attachment and subsequent infection by the bacterial parasite, Pasteuria ramosa. We discover a single locus with Mendelian segregation (3:1 ratio) with resistance being dominant, which we call the F locus. We use QTL analysis and fine mapping to localize the F locus to a 28.8-kb region in the host genome, adjacent to a known resistance supergene. We compare the 28.8-kb region in the two QTL parents to identify differences between host genotypes that are resistant versus susceptible to attachment and infection by the parasite. We identify 13 genes in the region, from which we highlight eight biological candidates for the F locus, based on presence/absence polymorphisms and differential gene expression. The top candidates include a fucosyltransferase gene that is only present in one of the two QTL parents, as well as several Cladoceran-specific genes belonging to a large family that is represented in multiple locations of the host genome. Fucosyltransferases have been linked to resistance in previous studies of Daphnia-Pasteuria and other host-parasite systems, suggesting that P. ramosa spore attachment could be mediated by changes in glycan structures on D. magna cuticle proteins. The Cladoceran-specific candidate genes suggest a resistance strategy that relies on gene duplication. Our results add a new locus to a growing genetic model of resistance in the D. magna-P. ramosa system. The identified candidate genes will be used in future functional genetic studies, with the ultimate aim to test for cycles of allele frequencies in natural populations.

Molecular evolution and depth-related adaptations of rhodopsin in the adaptive radiation of cichlid fishes in Lake Tanganyika.

The visual sensory system is essential for animals to perceive their environment and is thus under strong selection. In aquatic environments, light intensity and spectrum differ primarily along a depth gradient. Rhodopsin (RH1) is the only opsin responsible for dim-light vision in vertebrates and has been shown to evolve in response to the respective light conditions, including along a water depth gradient in fishes. In this study, we examined the diversity and sequence evolution of RH1 in virtually the entire adaptive radiation of cichlid fishes in Lake Tanganyika, focusing on adaptations to the environmental light with respect to depth. We show that Tanganyikan cichlid genomes contain a single copy of RH1. The 76 variable amino acid sites detected in RH1 across the radiation were not uniformly distributed along the protein sequence, and 31 of these variable sites show signals of positive selection. Moreover, the amino acid substitutions at 15 positively selected sites appeared to be depth-related, including three key tuning sites that directly mediate shifts in the peak spectral sensitivity, one site involved in protein stability and 11 sites that may be functionally important on the basis of their physicochemical properties. Among the strongest candidate sites for deep-water adaptations are two known key tuning sites (positions 292 and 299) and three newly identified variable sites (37, 104 and 290). Our study, which is the first comprehensive analysis of RH1 evolution in a massive adaptive radiation of cichlid fishes, provides novel insights into the evolution of RH1 in a freshwater environment.

Visual opsin gene expression evolution in the adaptive radiation of cichlid fishes of Lake Tanganyika.

Tuning the visual sensory system to the ambient light is essential for survival in many animal species. This is often achieved through duplication, functional diversification, and/or differential expression of visual opsin genes. Here, we examined 753 new retinal transcriptomes from 112 species of cichlid fishes from Lake Tanganyika to unravel adaptive changes in gene expression at the macro-evolutionary and ecosystem level of one of the largest vertebrate adaptive radiations. We found that, across the radiation, all seven cone opsins-but not the rhodopsin-rank among the most differentially expressed genes in the retina, together with other vision-, circadian rhythm-, and hemoglobin-related genes. We propose two visual palettes characteristic of very shallow- and deep-water living species, respectively, and show that visual system adaptations along two major ecological axes, macro-habitat and diet, occur primarily via gene expression variation in a subset of cone opsin genes.