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Turner, G. F.

Publications and source records attributed to Turner, G. F..

At least 19 recordsLinked to original sources

Genetic architecture of cichlid brain morphology

How evolutionary and developmental processes interact to determine axes of neural variation that produce behavioural diversity has been debated for many decades, with alternative hypotheses giving differential emphasis to functional coupling, which favours co-evolution, and developmental constraint, which enforces it. A critical omission is data on the genetic architecture of brain size and structure, which more closely illuminates the shared developmental dependencies between components of an integrated system. Here, we exploit ecological divergence between Astatotilapia calliptera and Aulonocara stuartgranti, two closely related cichlid species from Lake Malawi, to explore the genetic architecture of brain evolution. Using computer vision and machine learning techniques to extract volumetric data from micro-tomographic images, we first demonstrate significant divergence in brain composition between these species. Genomic and micro-tomographic imaging data from a population of hybrids generated between the two species were used to investigate genetic factors shaping this differentiation. We show that the majority of brain components are integrated phenotypically in hybrids, but genetic correlations between them are generally weaker. We further show that variation in multiple brain components is associated with variation in largely structure-specific quantitative trait loci, rather than determined by genetic factors with broad effects across the entire brain. These results suggest a genetic architecture that can facilitate modular changes in brain structure, and imply that individual components are independently evolvable.

evolutionary biology↗

Introgression dynamics of sex-linked chromosomal inversions shape the Malawi cichlid adaptive radiation

Chromosomal inversions contribute to adaptive speciation by linking co-adapted alleles. Querying 1,375 genomes of the species-rich Malawi cichlid fish radiation, we discovered five large inversions segregating in the benthic subradiation that each suppress recombination over more than half a chromosome. Two inversions were transferred from deepwater pelagic Diplotaxodon via admixture, while the others established early in the deep benthic clade. Introgression of haplotypes from lineages inside and outside the Malawi radiation coincided with bursts of species diversification. Inversions show evidence for transient sex linkage and a striking excess of protein changing substitutions points towards selection on neuro-sensory, physiological and reproductive genes. We conclude that repeated interplay between depth adaptation and sex-specific selection on large inversions has been central to the evolution of this iconic system.

evolutionary biology↗

Two new species of Mylochromis species (Cichlidae) from Lake Malawi, Africa

Two new species of Mylochromis Regan 1920 are described from specimens collected on shallow rocky habitats on the northwestern coast of Lake Malawi. The generic designation is based on their prominent oblique striped pattern and lack of any of the unique features of other Malawi cichlid genera with this pattern. Mylochromis rotundus sp. nov. is distinguished from most congeneric species by its relatively deep, rounded body and lack of enlarged pharyngeal teeth. It is further distinguished from M. semipalatus and M. melanonotus (if they are different species) by its relatively shorter snout. Mylochromis durophagus sp. nov. is distinguished from most congeneric species by its strongly molarised pharyngeal dentition. It differs from Mylochromis mola in having a shorter snout, less acutely pointed head profile, deeper body and in having a more continuous oblique stripe. Mylochromis durophagus has a much less steep head profile than Mylochromis anaphyrmus or Mylochromis sphaerodon. It is suggested that Mylochromis rotundus was previously identified informally as Mylochromis sp. mollis north, and M. durophagus as M. sp. mollis chitande. Lectotypes are designated for comparator species Mylochromis sphaerodon and Mylochromis subocularis.

zoology↗

Population genomic analysis reveals cryptic population structure in the commercially important Lake Malawi cichlid Copadichromis mloto

Fish is an important source of animal protein for many people living around Lake Malawi. The evaluation of population structure and genetic diversity can yield useful information for management and conservation of fish species but is complicated in Lake Malawi by the close genetic relatedness of species of the recent cichlid adaptive radiation. In this study, we analysed whole-genome sequencing data of "true utaka", a group of cichlids previously common in fisheries, but that has faced strong decline due to overfishing. Our analysis of 223 individuals collected from fishermens catches along the western shoreline of Lake Malawi confirmed that Copadichromis mloto (C. sp. "virginalis kajose") is the true utaka most targeted by fisheries. Genetic principal component analysis, phylogenetic inference, and admixture analysis revealed complex patterns of population structure. The presence of at least three geographically widespread genetic clades that have remained separate despite gene flow and partial sympatry hints at the presence of currently undescribed, cryptic species diversity in C. mloto. This result leads us to suggest that, despite the lack of obvious habitat barriers, benthic and pelagic species of Malawi cichlids might harbour unidentified species diversity and calls for further genetic and taxonomic research to define appropriate conservation units.

genomics↗

A pangenomic perspective of the Lake Malawi cichlid radiation reveals extensive structural variation driven by transposable elements

The East African Rift Lakes, namely Lake Malawi, Victoria, and Tanganyika, host a remarkable diversity of cichlid fishes, representing one of natures most striking vertebrate radiations. Despite rich phenotypic diversity, single nucleotide polymorphism (SNP)-based sequencing studies have revealed little sequence divergence between cichlids, with 0.1 to 0.25% pairwise divergence within Lake Malawi. These studies were based on aligning short reads to a single linear reference genome, which ignores the contribution of larger scale structural variants (SVs). To complement existing SNP-based studies, we adopted a pangenomic approach by constructing a multiassembly graph of haplochromine cichlids in Lake Malawi. We produced six new long read genome assemblies, alongside two publicly available ones, to span most of the major eco-morphological clades in the lake. This approach not only identifies longer SVs, but also visually represents complex and nested variation. Strikingly, the SV landscape is dominated by large insertions, many exclusive to individual assemblies. From a pangenomic perspective, we observed an exceptional amount of extra sequence, totaling up to 33.1% additional bases with respect to a single cichlid genome. Approximately 4.73 to 9.86% of the cichlid assemblies were estimated to be interspecies structural variation, suggesting substantial genomic diversity underappreciated in previous SNP-based studies. While coding regions remain highly conserved, our analysis uncovers a significant contribution of SVs from transposable element (TE) insertions, especially DNA, LINE, and LTR transposons. These findings underscore the intricate interplay of evolutionary forces shaping cichlid genome diversity, including both small nucleotide mutations and large TE-derived sequence alterations.

evolutionary biology↗

Rapid evolution of recombination landscapes during the divergence of cichlid ecotypes in Lake Masoko

Variation of recombination rate along the genome is of crucial importance to rapid adaptation and organismal diversification. Many unknowns remain regarding how and why recombination landscapes evolve in nature. Here, we reconstruct recombination maps based on linkage disequilibrium and use subsampling and simulations to derive a new measure of recombination landscape evolution: the Population Recombination Divergence Index (PRDI). Using PRDI, we show that fine-scale recombination landscapes differ substantially between two cichlid fish ecotypes of Astatotilapia calliptera that diverged only [~]2,500 generations ago. Perhaps surprisingly, recombination landscape differences are not driven by divergence in terms of allele frequency (FST) and nucleotide diversity ({Delta}({pi})): although there is some association, we observe positive PRDI in regions where FST and{Delta} ({pi}) are zero. We found a stronger association between evolution of recombination and 47 large haplotype blocks that are polymorphic in Lake Masoko, cover 21% of the genome, and appear to include multiple inversions. Among haplotype blocks, there is a strong and clear association between the degree of recombination divergence and differences between ecotypes in heterozygosity, consistent with recombination suppression in heterozygotes. Overall, our work provides a holistic view of changes in population recombination landscapes during early stages of speciation with gene flow.

evolutionary biology↗

A whole-body micro-CT scan library that captures the skeletal diversity of Lake Malawi cichlid fishes

Here we describe a dataset of freely available, readily processed, whole-body CT-scans of 56 species (116 specimens) of Lake Malawi cichlid fishes that captures a considerable majority of the morphological variation present in this remarkable adaptive radiation. We contextualise the scanned specimens within a discussion of their respective ecomorphological groupings and suggest possible macroevolutionary studies that could be conducted with these data. We also describe a methodology to efficiently CT-scan (on average) 23 specimens per hour, limiting scanning time and alleviating the financial cost whilst maintaining high resolution. We demonstrate the utility of this method by reconstructing 3D models of multiple bones from multiple specimens within the dataset. We hope this dataset will enable further morphological study of this fascinating system and permit wider-scale comparisons with other cichlid adaptive radiations.

evolutionary biology↗

Ancient and ongoing hybridization in the Oreochromis cichlid fishes

Hybridization may enable adaptive diversification by generating unique genetic combinations when hybrid lineages are faced with ecological opportunity. Conversely, hybridization with exotic species may be detrimental to native biodiversity, by leading to homogenisation and the loss of important genetic material associated with local adaptation. Here we studied both ancient and contemporary hybridization in cichlid fishes of the genus Oreochromis (tilapia), which are among the most important fish for global aquaculture. We use whole genome resequencing of 575 individuals from 23 species, focussing on Tanzania, a natural hotspot of tilapia diversity, and a country where hybridization between exotic and native species in the natural environment has been previously reported. We reconstruct the first genome-scale phylogeny of the genus and reveal prevalent ancient gene flow across the Oreochromis phylogeny. This introgression has not led to large-scale adaptive radiation as seen in other cichlid lineages. We identify multiple cases of contemporary hybridization between native and introduced species in the wild, linked to the use of non-native species in aquaculture improvement and stocking for capture fisheries. Our study shows how ancient hybridization contributed to modern tilapia diversity, but is now a threat to both the genetic integrity of wild populations and the long-term prospects of the global tilapia aquaculture industry.

evolutionary biology↗

A new species of Lethrinops (Cichliformes: Cichlidae) from a Lake Malawi satellite lake, believed to be extinct in the wild.

A new species of cichlid fish, Lethrinops chilingali is described from specimens collected from Lake Chilingali, near Nkhotakota, Malawi. It is assigned to the genus Lethrinops based on the form of the lower jaw dental arcade and by the absence of traits diagnostic of the phenotypically similar Ctenopharynx, Taeniolethrinops and Tramitichromis. It also lacks the enlarged cephalic lateral line canal pores found in species of Alticorpus and Aulonocara. The presence of a broken horizontal stripe on the flanks of females and immature/non-territorial males of Lethrinops chilingali distinguishes them from all congeners, including Lethrinops lethrinus, in which the stripe is typically continuous. Lethrinops chilingali also has a relatively shorter snout, shorter lachrymal bone and less ventrally positioned mouth than Lethrinops lethrinus. It appears likely that Lethrinops chilingali is now extinct in the wild, as this narrow endemic species has not been positively recorded in the natural environment since 2009. Breeding populations remain in captivity.

zoology↗

A new species of deepwater Lethrinops (Cichlidae) from Lake Malawi

A new species of cichlid fish, Lethrinops atrilabris is described from specimens collected by trawling at a depth of around 90m off Monkey Bay, southern Lake Malawi. It is assigned to the genus Lethrinops on the basis of its vertical flank barring, lack of enlarged cephalic lateral line canal pores and the form of the lower jaw dental arcade. It can be distinguished from congeneric species by its male breeding dress of contrasting flank barring and dark ventral surface, most strikingly on the lips, throat and chest, its relatively small known maximum size (<75mm SL), large eyes (38-41% head length), laterally compressed body (depth 2.5-2.7 times max head width) and lower gillraker count (13-14).

zoology↗

Taxonomic investigation of the zooplanktivorous Lake Malawi cichlids Copadichromis mloto (Iles) and C. virginalis (Iles).

The taxonomic status of the zooplanktivorous cichlids Copadichromis mloto and C. virginalis has been confused since their original descriptions by lles in 1960. While two forms of C. virginalis, Kaduna and Kajose, were distinguished in the type material, C. mloto has not been positively identified since its original description. Here we re-examined the types as well as 54 recently collected specimens from multiple sampling locations. Genome sequencing of 51 recent specimens revealed two closely related but reciprocally monophyletic clades. Geometric morphological analysis indicated that one clade morphologically encompasses the type specimens of C. virginalis identified by Iles as the Kaduna form, including the holotype, while the other clade encompasses not only the paratypes identified as the Kajose form, but also the type series of C. mloto. Given that all three forms have the same type locality, that there are no meristic or character states to differentiate them and that there are no records of adult male C. mloto in breeding colours, we conclude that the Kajose form previously identified as C. virginalis represents relatively deeper bodied sexually active or maturing individuals of C. mloto.

zoology↗

Ecological speciation promoted by divergent regulation of functional genes within African cichlid fishes

Rapid ecological speciation along depth gradients has taken place independently and repeatedly in freshwater fishes. While the extent of genomic divergence between ecomorphs is often well understood, the molecular mechanisms facilitating such rapid diversification are typically unclear. In Lake Masoko, an East African crater lake, the cichlid Astatotilapia calliptera has diverged into shallow littoral and deep benthic ecomorphs with strikingly different jaw structures within the last 1,000 years. Using genome-wide transcriptome data from jaw tissue, we explore two major regulatory transcriptional mechanisms, expression and splicing QTL variants and examine their contribution to differential gene expression underpinning functional phenotypes. We identified 7,550 genes with significant differential expression between ecomorphs, of which 4.2% were regulated by cis-regulatory expression QTLs, and 6.4% were regulated by cis-regulatory splicing QTLs. There were also strong signals of divergent selection of differentially expressed genes that showed divergent regulation from expression, splicing or both QTL variants, including genes associated with major jaw plasticity and adaptation networks, adaptive immune system response, and oxidoreductase processes. These results suggest that transcriptome plasticity and modification have important roles during early-stage ecological speciation and demonstrate the role of regulatory-variants as important targets of selection driving ecologically-relevant divergence in gene expression that is associated with adaptive diversification.

evolutionary biology↗

oca2 targeting using CRISPR/Cas9 in the Malawi cichlid Astatotilapia calliptera

Identifying genetic loci underlying trait variation provides insights into the mechanisms of diversification, but demonstrating causality and characterising the role of genetic loci requires testing candidate gene function, often in non-model species. Here we establish CRISPR/Cas9 editing in Astatotilapia calliptera, a generalist cichlid of the remarkably diverse Lake Malawi radiation. By targeting the gene oca2 required for melanin synthesis in other vertebrate species, we show efficient editing and germline transmission. Gene edits include indels in the coding region, likely a result of non-homologous end joining, and a large deletion in the 3' UTR due to homology-directed repair. We find that oca2 knock-out A. calliptera lack melanin, which may be useful for developmental imaging in embryos and studying colour pattern formation in adults. As A. calliptera resembles the presumed generalist ancestor of the Lake Malawi cichlids radiation, establishing genome editing in this species will facilitate investigating speciation, adaptation and trait diversification in this textbook radiation.

developmental biology↗

Differential use of multiple genetic sex determination systems in divergent ecomorphs of an African crater lake cichlid

African cichlid fishes not only exhibit remarkably high rates of speciation but also have some of the fastest evolving sex determination systems in vertebrates. However, little is known empirically in cichlids about the genetic mechanisms generating new sex-determining variants, what forces dictate their fate, the demographic scales at which they evolve, and whether they are related to speciation. To address these questions, we looked for sex-associated loci in full genome data from 647 individuals of Astatotilapia calliptera from Lake Masoko, a small isolated crater lake in Tanzania, which contains two distinct ecomorphs of the species. We identified three separate XY systems on recombining chromosomes. Two Y alleles derive from mutations that increase expression of the gonadal soma-derived factor gene (gsdf) on chromosome 7; the first is a tandem duplication of the entire gene observed throughout much of the Lake Malawi haplochromine cichlid radiation to which A. calliptera belongs, and the second is a 5 kb insertion directly upstream of gsdf. Both the latter variant and another 700 bp insertion on chromosome 19 responsible for the third Y allele arose from transposable element insertions. Males belonging to the Masoko deep-water benthic ecomorph are determined exclusively by the gsdf duplication, whereas all three Y alleles are used in the Masoko littoral ecomorph, in which they appear to act antagonistically among males with different amounts of benthic admixture. This antagonism in the face of ongoing admixture may be important for sustaining multifactorial sex determination in Lake Masoko. In addition to identifying the molecular basis of three coexisting sex determining alleles, these results demonstrate that genetic interactions between Y alleles and genetic background can potentially affect fitness and adaptive evolution.

evolutionary biology↗

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. We focus on the extent and functional relevance of DNA methylome divergence between two Astatotilapia calliptera ecomorphs in crater Lake Masoko, southern Tanzania. We report extensive genome-wide methylome divergence between populations linked to key biological processes, including transcriptional activity of ecologically-relevant genes. These include genes involved in steroid metabolism, haemoglobin composition and erythropoiesis, consistent with divergent habitat occupancy of the ecomorphs. Using a common garden experiment, we found that global methylation profiles are rapidly remodelled across generations, but ecomorph-specific differences can be inherited. Collectively, our study suggests an epigenetic contribution to early stages of vertebrate speciation. One sentence summaryInheritance and plasticity of epigenetic divergence characterise early stages of speciation in an incipient cichlid species of an African crater lake.

genomics↗

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 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 mores which are likely to result from reduced aggression. 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 ability of rare morphs to spend more time feeding. Reduced aggression to rare morph individuals by heterospecifics may also contribute to rare morph advantage.

evolutionary biology↗

Whole genome resequencing data enables a targeted SNP panel for conservation and aquaculture of Oreochromis cichlid fishes

Cichlid fish of the genus Oreochromis form the basis of the global tilapia aquaculture and fisheries industry. Non-native farmed tilapia populations are known to be widely distributed across Africa and to hybridize with native Oreochromis species. However, many species are difficult to distinguish morphologically, hampering attempts to maintain good quality farmed strains or to identify pure populations of native species. Here, we describe the development of a single nucleotide polymorphism (SNP) genotyping panel from whole-genome resequencing data that enables targeted species identification in Tanzania. We demonstrate that an optimized panel of 96 genome-wide SNPs based on FST outliers performs comparably to whole genome resequencing in distinguishing species and identifying hybrids. We also show this panel outperforms microsatellite-based and phenotype-based classification methods. Case studies indicate several locations where introduced aquaculture species have become established in the wild, threatening native Oreochromis species. The novel SNP markers identified here represent an important resource for assessing broodstock purity and helping to conserve unique endemic biodiversity, and in addition potentially for assessing broodstock purity in hatcheries.

evolutionary biology↗

The methylomes of Lake Malawi cichlids reveal epigenetic variation associated with phenotypic diversification

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.

evolutionary biology↗