bioRxiv Science⌕ Search

Biology subjects

Carleton, K. L.

Publications and source records attributed to Carleton, K. L..

6 recordsLinked to original sources

Parallel phenotypes underpinned by different genes in the visual system of two trans-isthmian coral reef fish species pairs

Understanding the genetic basis of adaptation in natural populations to changing environmental conditions is challenging. The relatively simple genotype-to-phenotype relationship between opsin genes and visual pigments offers a particularly informative model to explore the molecular mechanisms underpinning adaptive phenotypic change in natural populations. Here we leveraged the natural experiment provided by the tectonic closure of the Central American seaway that created allopatric, sister taxa in multiple, independent lineages of marine organisms and exposed them to distinct underwater light environments: either the more turbid Tropical Eastern Pacific (TEP), or the spectrally broader Caribbean Sea. Using two species pairs of planktivorous teleosts, the Azurina multilineata/A. atrilobata damselfish and the Cephalopholis (Paranthias) furcifer/C. colonus groupers, we explore to what extent visual sensitivity converged to similar adaptations in response to similar foraging strategies and shared underwater light in each marine basin. We found that the compression of the underwater light field towards the central portion of the spectrum from Caribbean to TEP waters is reflected in similar shifts towards the centre of the light spectrum in overall single and double cone sensitivities in both families. Both TEP species have single (short-wavelength) cone sensitivities shifted to longer wavelengths and double (long-wavelength) cone sensitivities shifted to shorter wavelengths, compared to their Caribbean counterparts. These parallel shifts in visual sensitivities observed in response to shared underwater light environments are accomplished by different underlying opsin gene toolsets in the two lineages. Similarly, expression changes in pathways associated with the visual system revealed limited parallelism at the molecular level.

evolutionary biology↗

Movement of transposable elements contributes to cichlid diversity

African cichlid fishes are a prime model for studying the mechanisms of speciation. Despite the development of extensive genomic resources, it has been difficult to determine which sources of genetic variation are responsible for variation in cichlid phenotypes. Cichlids have some of the largest known shifts in vertebrate visual sensitivity. These shifts arise mainly from the differential expression of seven cone opsin genes. By mapping expression quantitative trait loci (eQTL) in intergeneric crosses of Lake Malawi (LM) cichlids, we have thus far identified four causative genetic variants that correspond to indels in the promoters of either key transcription factors or of the opsin gene itself. Here we show that these indels are caused by the movement of transposable elements (TEs). These precise indels are not found outside of LM, suggesting that these TEs are recently active and are segregating within the Malawi cichlid lineage. A similar indel has arisen independently outside of LM at one locus, suggesting that some locations are primed for TE insertion and the resulting indels. Increased TE mobility may be associated with interspecific hybridization, which disrupt mechanisms of TE suppression. Overall, our study suggests that TEs may contribute to key regulatory changes, and may facilitate rapid phenotypic change and possibly speciation in African cichlids.

evolutionary biology↗

Visual pigment evolution in Characiformes: the dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning.

Vision represents an excellent model for studying adaptation, given the genotype-to-phenotype-map that has been characterized in a number of taxa. Fish possess a diverse range of visual sensitivities and adaptations to underwater light making them an excellent group to study visual system evolution. In particular, some speciose but understudied lineages can provide a unique opportunity to better understand aspects of visual system evolution such as opsin gene duplication and neofunctionalization. In this study, we characterized the visual system of Neotropical Characiformes, which is the result of several spectral tuning mechanisms acting in concert including gene duplications and losses, gene conversion, opsin amino acid sequence and expression variation, and A1/A2-chromophore shifts. The Characiforms we studied utilize three cone opsin classes (SWS2, RH2, LWS) and a rod opsin (RH1). However, the characiforms entire opsin gene repertoire is a product of dynamic evolution by opsin gene loss (SWS1, RH2) and duplication (LWS, RH1). The LWS- and RH1-duplicates originated from a teleost specific whole-genome duplication as well as characiform-specific duplication events. Both LWS-opsins exhibit gene conversion and, through substitutions in key tuning sites, one of the LWS-paralogs has acquired spectral sensitivity to green light. These sequence changes suggest reversion and parallel evolution of key tuning sites. In addition, characiforms exhibited species-specific differences in opsin expression. Finally, we found interspecific and intraspecific variation in the use of A1/A2-chromophores correlating with the light environment. These multiple mechanisms may be a result of the highly diverse visual environments where Characiformes have evolved.

evolutionary biology↗

Tbx2a modulates switching of opsin gene expression

Differences in sensory tuning are reported to maintain species boundaries and may even lead to speciation. Variation in the tuning of color vision is likely due to differences in the expression of opsin genes. Over 1,000 species of African cichlid fishes provide an excellent model system for studying the genetic basis of opsin gene expression because of the presence of seven distinct genes, yet individual species typically express only a divergent set of three opsins. The evolution of such shifts is expected to arise through either (a) two simultaneous regulatory changes (one for each opsin), or (b) one regulatory change that simultaneously promotes expression of one opsin while repressing another. Here, we used QTL analyses, genome sequencing, and gene expression studies to identify the transcription factor Tbx2a as likely driving a switch between LWS and RH2 opsin expression. Binding sites for Tbx2a in the LWS promoter and the highly conserved Locus Control Region of RH2 act to concurrently promote LWS expression while repressing RH2 expression. Our data support the hypothesis that instant changes in visual tuning can be achieved by switching the expression of multiple genes by a single mutation and do not require independent changes in the regulatory regions of each opsin.

evolutionary biology↗

Vision using multiple distinct rod opsins in deep-sea fishes

Vertebrate vision is accomplished through a set of light-sensitive photopigments, which are located in the photoreceptors of the retina and consist of a visual opsin protein bound to a chromophore. In dim-light, vertebrates generally rely upon a single rod opsin (RH1) for obtaining visual information. By inspecting 101 fish genomes, we found that three deep-sea teleost lineages have independently expanded their RH1 gene repertoires. Amongst these, the silver spinyfin (Diretmus argenteus Johnson 1863) stands out as having the highest number of visual opsins known for animals to date (2 cone and 38 rod opsins). Spinyfins simultaneously express up to 14 RH1s encoding for photopigments with different peak spectral sensitivities ({lambda}max=448-513 nm) that cover the range of the residual daylight, as well as the bioluminescence spectrum present in the deep-sea. Our findings present novel molecular and functional evidence for the recurrent evolution of multiple rod opsin-based vision in vertebrates.\n\nSHORT ABSTRACTContrary to the single rod opsin used by most vertebrates, some fishes use multiple rod opsins for vision in the dimly lit deep-sea.

evolutionary biology↗

Chromosome-scale assemblies reveal the structural evolution of African cichlid genomes

BackgroundAfrican cichlid fishes are well known for their rapid radiations and are a model system for studying evolutionary processes. Here we compare multiple, high-quality, chromosome-scale genome assemblies to understand the genetic mechanisms underlying cichlid diversification and study how genome structure evolves in rapidly radiating lineages.\n\nResultsWe re-anchored our recent assembly of the Nile tilapia (Oreochromis niloticus) genome using a new high-density genetic map. We developed a new de novo genome assembly of the Lake Malawi cichlid, Metriaclima zebra, using high-coverage PacBio sequencing, and anchored contigs to linkage groups (LGs) using four different genetic maps. These new anchored assemblies allow the first chromosome-scale comparisons of African cichlid genomes.\n\nLarge intra-chromosomal structural differences (~2-28Mbp) among species are common, while inter-chromosomal differences are rare (< 10Mbp total). Placement of the centromeres within chromosome-scale assemblies identifies large structural differences that explain many of the karyotype differences among species. Structural differences are also associated with unique patterns of recombination on sex chromosomes. Structural differences on LG9, LG11 and LG20 are associated with reductions in recombination, indicative of inversions between the rock- and sand-dwelling clades of Lake Malawi cichlids. M. zebra has a larger number of recent transposable element (TE) insertions compared to O. niloticus, suggesting that several TE families have a higher rate of insertion in the haplochromine cichlid lineage.\n\nConclusionThis study identifies novel structural variation among East African cichlid genomes and provides a new set of genomic resources to support research on the mechanisms driving cichlid adaptation and speciation.

genomics↗