Transcriptomes of aging brain, heart, muscle, and spleen from female and male African turquoise killifish.

The African turquoise killifish is an emerging vertebrate model organism with great potential for aging research due to its naturally short lifespan. Thus far, turquoise killifish aging 'omic' studies have examined a single organ, single sex and/or evaluated samples from non-reference strains. Here, we describe a resource dataset of ribosomal RNA-depleted RNA-seq libraries generated from the brain, heart, muscle, and spleen from both sexes, as well as young and old animals, in the reference GRZ turquoise killifish strain. We provide basic quality control steps and demonstrate the utility of our dataset by performing differential gene expression and gene ontology analyses by age and sex. Importantly, we show that age has a greater impact than sex on transcriptional landscapes across probed tissues. Finally, we confirm transcription of transposable elements (TEs), which are highly abundant and increase in expression with age in brain tissue. This dataset will be a useful resource for exploring gene and TE expression as a function of both age and sex in a powerful naturally short-lived vertebrate model.

Epigenetic divergence during early stages of speciation in an African crater lake cichlid fish.

Epigenetic variation can alter transcription and promote phenotypic divergence between populations facing different environmental challenges. Here, we assess the epigenetic basis of diversification during the early stages of speciation. Specifically, we focus on the extent and functional relevance of DNA methylome divergence in the very young radiation of Astatotilapia calliptera in crater Lake Masoko, southern Tanzania. Our study focuses on two lake ecomorphs that diverged approximately 1,000 years ago and a population in the nearby river from which they separated approximately 10,000 years ago. The two lake ecomorphs show no fixed genetic differentiation, yet are characterized by different morphologies, depth preferences and diets. We report extensive genome-wide methylome divergence between the two lake ecomorphs, and between the lake and river populations, linked to key biological processes and associated with altered transcriptional activity of ecologically relevant genes. Such genes differing between lake ecomorphs include those involved in steroid metabolism, hemoglobin composition and erythropoiesis, consistent with their divergent habitat occupancy. Using a common-garden experiment, we found that global methylation profiles are often rapidly remodeled across generations but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to the early stages of vertebrate speciation.

Mapping epigenetic divergence in the massive radiation of Lake Malawi cichlid fishes.

Epigenetic variation modulates gene expression and can be heritable. However, knowledge of the contribution of epigenetic divergence to adaptive diversification in nature remains limited. The massive evolutionary radiation of Lake Malawi cichlid fishes displaying extensive phenotypic diversity despite extremely low sequence divergence is an excellent system to study the epigenomic contribution to adaptation. Here, we present a comparative genome-wide methylome and transcriptome study, focussing on liver and muscle tissues in phenotypically divergent cichlid species. In both tissues we find substantial methylome divergence among species. Differentially methylated regions (DMR), enriched in evolutionary young transposons, are associated with transcription changes of ecologically-relevant genes related to energy expenditure and lipid metabolism, pointing to a link between dietary ecology and methylome divergence. Unexpectedly, half of all species-specific DMRs are shared across tissues and are enriched in developmental genes, likely reflecting distinct epigenetic developmental programmes. Our study reveals substantial methylome divergence in closely-related cichlid fishes and represents a resource to study the role of epigenetics in species diversification.

Rare morph Lake Malawi mbuna cichlids benefit from reduced aggression from con- and hetero-specifics.

Balancing selection is important for the maintenance of polymorphism as it can prevent either fixation of one morph through directional selection or genetic drift, or speciation by disruptive selection. Polychromatism, the presence of multiple genetically determined colour phenotypes, can be maintained if the fitness of alternative morphs depends on the relative frequency in a population. In aggressive species, negative frequency-dependent antagonism can prevent an increase in the frequency of rare morphs as they would only benefit from increased fitness while they are rare. Heterospecific aggression is common in nature and has the potential to contribute to rare morph advantage. Here we carry out field observations and laboratory aggression experiments with mbuna cichlids from Lake Malawi, to investigate the role of con- and heterospecific aggression in the maintenance of polychromatism and identify benefits to rare morphs which are likely to result from reduced aggression. We hypothesize that rare morph individuals receive less aggression than common morph individuals and therefore have an ecological advantage. Within species we found that males and females bias aggression towards their own morph, adding to the evidence that inherent own-morph aggression biases can contribute to balancing selection. Over-representation of rare morph territory owners may be influenced by two factors; higher tolerance of different morph individuals as neighbours, and the ability of rare morphs to spend more time feeding. Reduced aggression to rare morph individuals by heterospecifics may also contribute to rare morph advantage.

Ancestral transoceanic colonization and recent population reduction in a nonannual killifish from the Seychelles archipelago.

Whether freshwater fish colonize remote islands following tectonic or transoceanic dispersal remains an evolutionary puzzle. Integrating dating of known tectonic events with phylogenomics and current species distribution, we find that killifish species distribution is not explained by species dispersal by tectonic drift only. Investigating the colonization of a nonannual killifish (golden panchax, Pachypanchax playfairii) on the Seychelle islands, we found genetic support for transoceanic dispersal and experimentally discovered an adaptation to complete tolerance to seawater. At the macroevolutionary scale, despite their long-lasting isolation, nonannual golden panchax show stronger genome-wide purifying selection than annual killifishes from continental Africa. However, progressive decline in effective population size over a more recent timescale has probably led to the segregation of slightly deleterious mutations across golden panchax populations, which represents a potential threat for species preservation in the long term.

Widespread colonisation of Tanzanian catchments by introduced Oreochromis tilapia fishes: the legacy from decades of deliberate introduction.

From the 1950s onwards, programmes to promote aquaculture and improve capture fisheries in East Africa have relied heavily on the promise held by introduced species. In Tanzania these introductions have been poorly documented. Here we report the findings of surveys of inland water bodies across Tanzania between 2011 and 2017 that clarify distributions of tilapiine cichlids of the genus Oreochromis. We identified Oreochromis from 123 sampling locations, including 14 taxa restricted to their native range and three species that have established populations beyond their native range. Of these three species, the only exotic species found was blue-spotted tilapia (Oreochromis leucostictus), while Nile tilapia (Oreochromis niloticus) and Singida tilapia (Oreochromis esculentus), which are both naturally found within the country of Tanzania, have been translocated beyond their native range. Using our records, we developed models of suitable habitat for the introduced species based on recent (1960-1990) and projected (2050, 2070) East African climate. These models indicated that presence of suitable habitat for these introduced species will persist and potentially expand across the region. The clarification of distributions provided here can help inform the monitoring and management of biodiversity, and inform policy related to the future role of introduced species in fisheries and aquaculture.

Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow.

The hundreds of cichlid fish species in Lake Malawi constitute the most extensive recent vertebrate adaptive radiation. Here we characterize its genomic diversity by sequencing 134 individuals covering 73 species across all major lineages. The average sequence divergence between species pairs is only 0.1-0.25%. These divergence values overlap diversity within species, with 82% of heterozygosity shared between species. Phylogenetic analyses suggest that diversification initially proceeded by serial branching from a generalist Astatotilapia-like ancestor. However, no single species tree adequately represents all species relationships, with evidence for substantial gene flow at multiple times. Common signatures of selection on visual and oxygen transport genes shared by distantly related deep-water species point to both adaptive introgression and independent selection. These findings enhance our understanding of genomic processes underlying rapid species diversification, and provide a platform for future genetic analysis of the Malawi radiation.

Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake.

The genomic causes and effects of divergent ecological selection during speciation are still poorly understood. Here we report the discovery and detailed characterization of early-stage adaptive divergence of two cichlid fish ecomorphs in a small (700 meters in diameter) isolated crater lake in Tanzania. The ecomorphs differ in depth preference, male breeding color, body shape, diet, and trophic morphology. With whole-genome sequences of 146 fish, we identified 98 clearly demarcated genomic "islands" of high differentiation and demonstrated the association of genotypes across these islands with divergent mate preferences. The islands contain candidate adaptive genes enriched for functions in sensory perception (including rhodopsin and other twilight-vision-associated genes), hormone signaling, and morphogenesis. Our study suggests mechanisms and genomic regions that may play a role in the closely related mega-radiation of Lake Malawi.