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Genner, M. J.

Publications and source records attributed to Genner, M. J..

13 recordsLinked to original sources

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↗

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↗

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↗

Estuarine molecular bycatch as a landscape-wide biomonitoring tool

Environmental DNA analysis is rapidly transforming biodiversity monitoring and bolstering conservation applications worldwide. This approach has been assisted by the development of metabarcoding PCR primers that are suited for detection of a wide range of taxa. However, little effort has gone into exploring the value of the non-target DNA sequences that are generated in every survey, but subsequently discarded. Here we demonstrate that fish-targeted markers widely employed in aquatic biomonitoring can also detect birds and mammals present in the surrounding habitats. We showcase this feature in three temperate estuaries over multiple seasons, where dozens of bird and mammal species offer valuable insights into spatial and temporal faunal variation. Our results indicate that existing metabarcode sequence data sets are suitable for mining and exploration of this molecular by-catch, and that any future eDNA-based surveys can be designed to accommodate this enhanced property of this widely applicable tool.

ecology↗

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↗

Newly discovered tilapia cichlid fish biodiversity threatened by hybridization with non-native species

Invasive freshwater fish systems are known to readily hybridize with indigenous congeneric species, driving loss of unique and irreplaceable genetic resources. Here we reveal that newly discovered (2013-2016) evolutionarily significant populations of Korogwe tilapia (Oreochromis korogwe) from southern Tanzania are threatened by hybridization with the larger invasive Nile tilapia (Oreochromis niloticus). We use a combination of morphology, microsatellite allele frequencies and whole genome sequences to show that O. korogwe from southern lakes (Nambawala, Rutamba and Mitupa) are distinct from geographically-disjunct populations in northern Tanzania (Zigi River and Mlingano Dam). We also provide genetic evidence of O. korogwe x niloticus hybrids in three lakes and demonstrate heterogeneity in the extent of admixture across the genome. Finally, using the least admixed genomic regions we estimate that the northern and southern O. korogwe populations most plausibly diverged approximately 140,000 years ago, suggesting that the geographical separation of the northern and southern groups is not a result of a recent translocation, and instead these populations represent independent evolutionarily significant units. We conclude that these newly-discovered and phenotypically unique cichlid populations are already threatened by hybridization with an invasive species, and propose that these irreplaceable genetic resources would benefit from conservation interventions.

zoology↗

Relative growth of invasive and indigenous tilapiine cichlid fishes in Tanzania

Non-native species have been widely distributed across Africa for the enhancement of capture fisheries, but it can be unclear what benefits in terms of fisheries production the non-native species bring over native species. Here we compared the relative growth rate of sympatric populations of introduced Oreochromis niloticus (Nile tilapia) to indigenous Oreochromis jipe (Jipe tilapia) at three impoundments in Northern Tanzania. Using scale increments as a proxy for growth, we found that O. niloticus had an elevated growth rate relative to O. jipe, with the greatest O. niloticus growth rates being evident in the Nyumba ya Mungu reservoir. These results help explain why O. niloticus may be a superior competitor to native species in some circumstances. However, further introductions of this non-native species should be undertaken with caution given potential for negative ecological impacts on threatened indigenous tilapia species.

ecology↗

A survey of fishes of Hombolo Lake, Dodoma, Tanzania, with evidence for local extinction of a native tilapia as a consequence of stocking

The fish community of the Hombolo Lake, an impoundment on the Wami catchment near Dodoma, Tanzania, was surveyed in 2014 and 2017. The lake contains a relatively low diversity community dominated by two Oreochromis species introduced from outside the Wami catchment, O. niloticus and O. esculentus. Evidence from historical collections suggests that the native O. urolepis was formerly present, and its current absence is likely to be the result of competitive exclusion or genetic swamping by non-native species introduced for fishery enhancement. Four other fish species were also recorded.

ecology↗

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. 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.\n\nOne Sentence Summary: The genomes of 73 cichlid fish species from Lake Malawi uncover evolutionary processes underlying a large adaptive evolutionary radiation.

evolutionary biology↗

The genomic basis of adaptation to the deep water ‘twilight zone’ in Lake Malawi cichlid fishes

Deep water environments are characterized by low levels of available light at increasingly narrow spectra, great hydrostatic pressure and reduced dissolved oxygen - conditions predicted to exert highly specific selection pressures. In Lake Malawi over 800 cichlid species have evolved, and this adaptive radiation extends into the \"twilight zone\" below 100 metres. We use population-level RAD-seq data to investigate whether four endemic deep water species (Diplotaxodon spp.) have experienced divergent selection within this environment. We identify candidate genes including regulators of photoreceptor function, photopigments, lens morphology and haemoglobin, many not previously implicated in cichlid adaptive radiations. Co-localization of functionally linked genes suggests co-adapted \"supergene\" complexes. Comparisons of Diplotaxodon to the broader Lake Malawi radiation using genome resequencing data revealed functional substitutions in candidate genes. Our data provide unique insights into genomic adaptation to life at depth, and suggest genome-level specialisation for deep water habitat as an important process in cichlid radiation.

evolutionary biology↗