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Papers by Richard Nichols

Clonal propagation enables favourable crop genotypes to be rapidly selected and multiplied. Howev... more Clonal propagation enables favourable crop genotypes to be rapidly selected and multiplied. However, the absence of sexual propagation can lead to low genetic diversity and accumulation of deleterious mutations, which may eventually render crops less resilient to pathogens or environmental change. To better understand this trade-off, we characterise the domestication and contemporary genetic diversity of Enset (Ensete ventricosum), an indigenous African relative of bananas (Musa) and principal starch staple for 20 million Ethiopians. Wild enset is strictly sexually outcrossing, but in cultivation is exclusively propagated clonally and associated with diversification and specialisation into hundreds of named landraces. We applied tGBS sequencing to generate genome-wide genotypes for 192 accessions from across enset’s cultivated distribution, and surveyed 1340 farmers on enset agronomic traits. Overall, reduced heterozygosity in the domesticated lineage was consistent with a domestica...

Ecological Applications, 2021

Molecular Biology and Evolution, 2013

Evolutionary responses to sudden changes in the environment can, in theory, be rapid if they invo... more Evolutionary responses to sudden changes in the environment can, in theory, be rapid if they involve small shifts in allele frequencies at many loci. Such adaptation has proven hard to characterise in wild populations. We overcome these problems, in quantifying the genetic response of European ash trees (Fraxinus excelsior) to the strong selective challenge imposed by the invasive alien fungal pathogenHymenoscyphus fraxineus, by exploiting a previous study that had estimated effect sizes for many single nucleotide polymorphism (SNP) loci associated with resistance to the fungus in large field trials. We ask if the selective response, in a new natural setting of a multigenerational wild ash woodland, involves allele frequency changes at the 10,000 loci which provided the best genomic prediction of resistance in the field trials. We conducted whole genome resequencing of each tree and calculated its genetic merit as a Genomic Estimated Breeding Value (GEBV), using the previous estimat...

Proceedings of the Royal Society B: Biological Sciences, 2019

Angiosperm genome sizes (GS) varyca2400-fold. Recent research has shown that GS influences plant ... more Angiosperm genome sizes (GS) varyca2400-fold. Recent research has shown that GS influences plant abundance, and plant competition. There are also tantalizing reports that herbivores may select plants as food dependent on their GS. To test the hypothesis that GS plays a role in shaping plant communities under herbivore pressure, we exploit a grassland experiment that has experimentally excluded herbivores and applied nutrient over 8 years. Using phylogenetically informed statistical models and path analyses, we show that under rabbit grazing, plant species with small GS generated the most biomass. By contrast, on mollusc and insect-grazed plots, it was the plant species with larger GS that increased in biomass. GS was also shown to influence plant community properties (e.g. competitive strategy, total biomass) although the impact varied between different herbivore guilds (i.e. rabbits versus invertebrates) and nutrient inputs. Overall, we demonstrate that GS plays a role in influenci...

Genetics, Oct 1, 2006

Eukaryote nuclear ribosomal DNA (rDNA) typically exhibits strong concerted evolution: a pattern i... more Eukaryote nuclear ribosomal DNA (rDNA) typically exhibits strong concerted evolution: a pattern in which several hundred rDNA sequences within any one species show little or no genetic diversity, whereas the sequences of different species diverge. We report a markedly different pattern in the genome of the grasshopper Podisma pedestris. Single individuals contain several highly divergent ribosomal DNA groups. Analysis of the magnitude of divergence indicates that these groups have coexisted in the Podisma lineage for at least 11 million years. There are two putatively functional groups, each estimated to be at least 4 million years old, and several pseudogene groups, many of which are transcribed. Southern hybridization and realtime PCR experiments show that only one of the putatively functional types occurs at high copy number. However, this group is scarcely amplified under standard PCR conditions, which means that phylogenetic inference on the basis of standard PCR would be severely distorted. The analysis suggests that concerted evolution has been remarkably ineffective in P. pedestris. We propose that this outcome may be related to the species' exceptionally large genome and the associated low rate of deletion per base pair, which may allow pseudogenes to persist.

Molecular Phylogenetics and Evolution, Feb 1, 2014

Eurasian fauna. To investigate their controversial taxonomy and evolutionary history, we studied ... more Eurasian fauna. To investigate their controversial taxonomy and evolutionary history, we studied 86%, 33 78% and 33% respectively of the Eurasian, European and Asian Palaearctic genera (Otte, 1995; Eades 34 et al., 2013). We reconstructed parsimony, maximum likelihood and Bayesian phylogenies using frag-35 ments of four genes (ITS1, 16S, 12S, CO2). We applied a Bayesian molecular clock to estimate the times 36 of species divergence, and the event-based parsimony method to depict the biogeographic framework of 37 the diversification. Our results suggest that the selected Eurasian Podismini constitute a monophyletic 38 group inside the Melanoplinae, provided it includes the North American genus Phaulotettix. The clades 39 proposed by the present study inside the Podismini do not fit the older morphological or cytological clas-40 sifications, but are in agreement with more recent proposals. Furthermore, our results can be explained 41 by a plausible biogeographic history in which the present geographical distribution of the Eurasian Podis-42 mini resulted from known changes, to the Cenozoic climate and vegetation, induced by major geological 43 events including the genesis of high mountain chains (e.g., Himalayas, Altay, Alps) and large deserts (e.g.,

Journal for Nature Conservation, Dec 1, 2013

Policy makers and managers are increasingly called upon to assess the state of biodiversity, and ... more Policy makers and managers are increasingly called upon to assess the state of biodiversity, and make decisions regarding potential interventions. Genetic tools are well-recognized in the research community as a powerful approach to evaluate species and population status, reveal ecological and demographic processes, and inform nature conservation decisions. The wealth of genetic data and power of genetic methods are rapidly growing, but the consideration of genetic information and concerns in policy and management is limited by currently low capacity of decision-makers to access and apply genetic resources. Here we describe a freely-available, user-friendly online resource for decision-makers at local and national levels (http://congressgenetics.eu), which increases access to current knowledge, facilitates implementation of studies and interpretation of available data, and fosters collaboration between researchers and practitioners. This resource was created in partnership with conservation practitioners across the European Union, and includes a spectrum of taxa, ecosystems and conservation issues. Our goals here are to (1) introduce the rationale and context, (2) describe the specific tools (knowledge summaries, publications database, decision making tool, project planning tool, forum, community directory), and the challenges they help solve, and (3) summarize lessons learned. This articles provides an outlook and model for similar efforts to build policy and management capacity.

eLife, 2020

Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombin... more Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young ‘social’ supergene of fire ants, a powerful system for disentangling the effects of evolutionary antagonism and suppressed recombination. We hypothesize that gene degeneration and social antagonism shaped the evolution of the fire ant supergene, resulting in distinct patterns of gene expression. We test these ideas by identifying allelic differences between supergene variants, characterizing allelic expression across populations, castes and body parts, and contrasting allelic expression biases with differences in expression between social forms. We find strong signatures of gene degeneration and gene-specific dosage compensation. On this background, a small portion of the genes has the signature of adaptive responses to evoluti...

Nuclear inserts derived from mitochondrial DNA (Numts) encode valuable information. Being mostly ... more Nuclear inserts derived from mitochondrial DNA (Numts) encode valuable information. Being mostly non-functional, and accumulating mutations more slowly than mitochondrial sequence, they act like molecular fossils - they preserve information on the ancestral sequences of the mitochondrial DNA. In addition, changes to the Numt sequence since their insertion into the nuclear genome carry information about the nuclear phylogeny. These attributes cannot be reliably exploited if Numt sequence is confused with the mitochondrial genome (mtDNA). The analysis of mtDNA would be similarly compromised by any confusion, for example producing misleading results in DNA barcoding that used mtDNA sequence. We propose a method to distinguish Numts from mtDNA, without the need for comprehensive assembly of the nuclear genome or the physical separation of organelles and nuclei. It exploits the different biases of long and short-read sequencing. We find that short-read data yield mainly mtDNA sequences, ...

Global Change Biology, 2019

The global trend of increasing environmental temperatures is often predicted to result in more se... more The global trend of increasing environmental temperatures is often predicted to result in more severe disease epidemics. However, unambiguous evidence that temperature is a driver of epidemics is largely lacking, because it is demanding to demonstrate its role among the complex interactions between hosts, pathogens, and their shared environment. Here, we apply a three‐pronged approach to understand the effects of temperature on ranavirus epidemics in UK common frogs, combining in vitro, in vivo, and field studies. Each approach suggests that higher temperatures drive increasing severity of epidemics. In wild populations, ranavirosis incidents were more frequent and more severe at higher temperatures, and their frequency increased through a period of historic warming in the 1990s. Laboratory experiments using cell culture and whole animal models showed that higher temperature increased ranavirus propagation, disease incidence, and mortality rate. These results, combined with climate ...

SummaryPopulations of European ash trees (Fraxinus excelsior) are being devastated by the invasiv... more SummaryPopulations of European ash trees (Fraxinus excelsior) are being devastated by the invasive alien fungusHymenoscyphus fraxineus, which causes ash dieback (ADB). We sequenced whole genomic DNA from 1250 ash trees in 31 DNA pools, each pool containing trees with the same ADB damage status in a screening trial and from the same seed-source zone. A genome-wide association study (GWAS) identified 3,149 single nucleotide polymorphisms (SNPs) associated with low versus high ADB damage. Sixty-one of the 203 most significant SNPs were in, or close to, genes with putative homologs already known to be involved in pathogen responses in other plant species. We also used the pooled sequence data to train a genomic prediction (GP) model, cross-validated using individual whole genome sequence data generated for 75 healthy and 75 damaged trees from a single seed source. Using the top 30% of our genomic estimated breeding values from 200 SNPs, we could predict tree health with over 90% accurac...

Increasing environmental temperatures are predicted to have increasingly severe and deleterious e... more Increasing environmental temperatures are predicted to have increasingly severe and deleterious effects on biodiversity. For the most part, the impacts of a warming environment are presumed to be direct, however some predict increasingly severe disease epidemics, primarily from vector-borne pathogens, that will have the capacity to deplete host populations. Data to support this hypothesis are lacking. Here we describe increasing severity of ranavirosis driven by increasing temperature affecting a widely distributed amphibian host. Both in vitro and in vivo experiments showed that increasing environmental temperature leads to increased propagation of ranavirus and, in the latter, increased incidence of host infection and mortality. Also, temperature was shown to be a key determinant of disease dynamics in wild amphibians, raising the odds and severity of disease incidents. The direction of this effect was highly consistent in the context of other interacting variables such as shading...

Heredity, 2018

Dwarf birch (Betula nana) has a widespread boreal distribution but has declined significantly in ... more Dwarf birch (Betula nana) has a widespread boreal distribution but has declined significantly in Britain where populations are now highly fragmented. We analyzed the genetic diversity of these fragmented populations using markers that differ in mutation rate: conventional microsatellites markers (PCR-SSRs), RADseq generated transition and transversion SNPs (RAD-SNPs), and microsatellite markers mined from RADseq reads (RAD-SSRs). We estimated the current population sizes by census and indirectly, from the linkage-disequilibrium found in the genetic surveys. The two types of estimate were highly correlated. Overall, we found genetic diversity to be only slightly lower in Britain than across a comparable area in Scandinavia where populations are large and continuous. While the ensemble of British fragments maintain diversity levels close to Scandinavian populations, individually they have drifted apart and lost diversity; particularly the smaller populations. An ABC analysis, based on coalescent models, favors demographic scenarios in which Britain maintained high levels of genetic diversity through post-glacial re-colonization. This diversity has subsequently been partitioned into population fragments that have recently lost diversity at a rate corresponding to the current population-size estimates. We conclude that the British population fragments retain sufficient genetic resources to be the basis of conservation and replanting programmes. Use of markers with different mutation rates gives us greater confidence and insight than one marker set could have alone, and we suggest that RAD-SSRs are particularly useful as high mutation-rate marker set with a wellspecified ascertainment bias, which are widely available yet often neglected in existing RAD datasets.

Molecular Ecology, 2017

Variation in social behaviour is common, yet little is known about the genetic architectures unde... more Variation in social behaviour is common, yet little is known about the genetic architectures underpinning its evolution. A rare exception is in the fire ant Solenopsis invicta: Alternative variants of a supergene region determine whether a colony will have exactly one or up to dozens of queens. The two variants of this region are carried by a pair of ‘social chromosomes’, SB and Sb, which resemble a pair of sex chromosomes. Recombination is suppressed between the two chromosomes in the supergene region. While the X‐like SB can recombine with itself in SB/SB queens, recombination is effectively absent in the Y‐like Sb because Sb/Sb queens die before reproducing. Here, we analyse whole‐genome sequences of eight haploid SB males and eight haploid Sb males. We find extensive SB–Sb differentiation throughout the >19‐Mb‐long supergene region. We find no evidence of ‘evolutionary strata’ with different levels of divergence comparable to those reported in several sex chromosomes. A high ...

Proceedings of the Royal Society B: Biological Sciences, 2016

There have been few reconstructions of wildlife disease emergences, despite their extensive impac... more There have been few reconstructions of wildlife disease emergences, despite their extensive impact on biodiversity and human health. This is in large part attributable to the lack of structured and robust spatio-temporal datasets. We overcame logistical problems of obtaining suitable information by using data from a citizen science project and formulating spatio-temporal models of the spread of a wildlife pathogen (genusRanavirus, infecting amphibians). We evaluated three main hypotheses for the rapid increase in disease reports in the UK: that outbreaks were being reported more frequently, that climate change had altered the interaction between hosts and a previously widespread pathogen, and that disease was emerging due to spatial spread of a novel pathogen. Our analysis characterized localized spread from nearby ponds, consistent with amphibian dispersal, but also revealed a highly significant trend for elevated rates of additional outbreaks in localities with higher human popula...

A key quantity in the analysis of structured populations is the parameter K, which describes the ... more A key quantity in the analysis of structured populations is the parameter K, which describes the number of subpopulations that make up the total population. Inference of K ideally proceeds via the model evidence, which is equivalent to the likelihood of the model. However, the evidence in favour of a particular value of K cannot usually be computed exactly, and instead programs such as STRUCTURE make use of simple heuristic estimators to approximate this quantity. We show - using simulated data sets small enough that the true evidence can be computed exactly - that these simple heuristics often fail to estimate the true evidence, and that this can lead to incorrect conclusions about K. Our proposed solution is to use thermodynamic integration (TI) to estimate the model evidence. After outlining the TI methodology we demonstrate the effectiveness of this approach using a range of simulated data sets. We find that TI can be used to obtain estimates of the model evidence that are order...

Heredity, 1986

Chiasma variation has been studied in two selected chromosomes from two species of the genus Arcy... more Chiasma variation has been studied in two selected chromosomes from two species of the genus Arcyptera according to the heterochromatin distribution per bivalent. The differences in chiasma distribution found between each karyomorph revealed an underlying tendency for chiasmata to occupy characteristic positions in the bivalents depending on the heterochromatin distribution. It seems that the heterozygosity of the bivalent more than the presence of heterochromatic segments is readjusting a standard pattern of chiasma distribution. The findings of this survey are discussed in relation to the significance and role of genetical recombination in natural populations depending on the frequency of karyomorphs per populations and the pattern of chiasma distribution per individual.

Evolutionary Journal of the Linnean Society

The bluebells Hyacinthoides hispanica (Mill.) Rothm. and H. non-scripta (L.) Chouard ex Rothm. fo... more The bluebells Hyacinthoides hispanica (Mill.) Rothm. and H. non-scripta (L.) Chouard ex Rothm. form a hybrid zone in Spain and represent a natural experiment for the study of gene flow between species. The results of this study provide not only important insights to obtain empirical evidence regarding the mechanisms of gene flow enabled by hybridization but also to improve conservation assessment of the anthropogenic hybridization zone amongst bluebells occurring in Britain. We developed genome-wide genetic markers for amplicon-based resequencing from individuals across the hybrid zone, mapped morphological changes across the zone and determined the fitness of hybrids in laboratory crosses. We revealed significant clines across the zone at 61% of single nucleotide polymorphisms of the nuclear genes, most of which have a relatively shallow slope (mean slope 0.051 km–1, mean width of 78.4 km). In contrast, there was a rapid change in organellar haplotypes (slope = 0.238 km–1, mean wid...

PLoS Genetics, 2007

Comparisons of the DNA sequences of metazoa show an excess of transitional over transversional su... more Comparisons of the DNA sequences of metazoa show an excess of transitional over transversional substitutions. Part of this bias is due to the relatively high rate of mutation of methylated cytosines to thymine. Postmutation processes also introduce a bias, particularly selection for codon-usage bias in coding regions. It is generally assumed, however, that there is a universal bias in favour of transitions over transversions, possibly as a result of the underlying chemistry of mutation. Surprisingly, this underlying trend has been evaluated only in two types of metazoan, namely Drosophila and the Mammalia. Here, we investigate a third group, and find no such bias. We characterize the point substitution spectrum in Podisma pedestris, a grasshopper species with a very large genome. The accumulation of mutations was surveyed in two pseudogene families, nuclear mitochondrial and ribosomal DNA sequences. The cytosine-guanine (CpG) dinucleotides exhibit the high transition frequencies expected of methylated sites. The transition rate at other cytosine residues is significantly lower. After accounting for this methylation effect, there is no significant difference between transition and transversion rates. These results contrast with reports from other taxa and lead us to reject the hypothesis of a universal transition/transversion bias. Instead we suggest fundamental interspecific differences in point substitution processes.