Movement of transposable elements contributes to cichlid diversity

Abstract

African cichlid fishes are a prime model for studying speciation mechanisms. Despite the development of extensive genomic resources, it has been difficult to determine which sources of genetic variation are responsible for cichlid phenotypic variation. One of their most variable phenotypes is visual sensitivity, with some of the largest spectral shifts among vertebrates. These shifts arise primarily from differential expression of seven cone opsin genes. By mapping expression quantitative trait loci (eQTL) in intergeneric crosses of Lake Malawi cichlids, we previously identified four causative genetic variants that correspond to indels in the promoters of either key transcription factors or an opsin gene. In this comprehensive study, we show that these indels are the result of the movement of transposable elements (TEs) that correlate with opsin expression variation across the Malawi flock. In tracking the evolutionary history of these particular indels, we found they are endemic to Lake Malawi, suggesting that these TEs are recently active and are segregating within the Malawi cichlid lineage. However, an independent indel has arisen at a similar genomic location in one locus outside of the Malawi flock. The convergence in TE movement suggests these loci are primed for TE insertion and subsequent deletions. Increased TE mobility may be associated with interspecific hybridization, which disrupts mechanisms of TE suppression. This might provide a link between cichlid hybridization and accelerated regulatory variation. Overall, our study suggests that TEs may be an important driver of key regulatory changes, facilitating rapid phenotypic change and possibly speciation in African cichlids.

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

“…Even though most of TE activity is under tight cellular control to ensure genome stability, transposition events have also been associated with genome evolution and phenotypic diversification. Indeed, TE insertion may represent a source of functional genomic variation and novel cis -regulatory elements, underlying altered transcriptional network 44,46,47,63 . In haplochromine cichlids, variation in anal fin egg-spots patterns associated with courtship behaviour, has been linked to a novel cis -regulatory element, derived from TE sequences 45 .…”

“…Differential methylation in TE sequences may affect their transcription and transposition activities, possibly altering or establishing new transcriptional activity networks via cis-regulatory functions [44][45][46] . Indeed, movement of transposable elements has recently been shown to contribute to phenotypic diversification in Lake Malawi cichlids 47 .…”

Multiple ancestral duplications of the red-sensitive opsin gene (LWS) in teleost fishes and convergent spectral shifts to green vision in gobies

“…These five types were already present in the vertebrate ancestor and are thought to be the product of two rounds of whole-genome duplication (2R) ~ 500 million years ago (Mya) (Lamb, 2013). They are the dim-light active rod opsin (rhodopsin; RH1) which typically operates in the blue-green light spectrum [peak spectral sensitivity (λ max ) ~ 445 to 525nm], and four differently tuned cone opsins: short-wavelength-sensitive 1 and 2 (SWS1: λ max ~ 345 to 440 nm; SWS2: λ max ~ 395 to 490 nm), rhodopsin-like 2 (RH2: λ max ~ 450 to 540 nm), and mid/long-wavelength-sensitive (MWS/LWS: λ max ~ 490 to 575 nm) (Yokoyama 2008; Carleton et al 2020). The different cone-based photopigments are active during bright-light conditions where they are often involved in colour vision (Hunt et al 2014).…”

“…The evolution of vertebrate visual opsins is characterised by changes in opsin gene numbers, gene structure and gene expression (Hunt et al 2014; Lamb 2019). Unlike in terrestrial vertebrates, where the basic opsin setup was either maintained [e.g., birds (Borges et al, 2015), reptiles (Katti et al, 2019)] or reduced [e.g., mammals (Jacobs, 2013)], opsin genes have continued to proliferate in teleost fishes (reviewed in Carleton et al 2020 and Musilova et al, 2021) – with nearly 35,000 species, the most species-rich clade of vertebrates (Fricke et al, 2021). Teleosts are extremely diverse in ecology, physiology and morphology as they have conquered almost every aquatic habitat (few species have even transitioned to land) from clear mountain streams to the relative darkness of the deep-sea.…”

“…Teleosts are extremely diverse in ecology, physiology and morphology as they have conquered almost every aquatic habitat (few species have even transitioned to land) from clear mountain streams to the relative darkness of the deep-sea. It is those differences in photic environment and life history traits that are the main drivers for opsin gene diversity and evolution in fishes (Carleton et al 2020).…”