Editors' Choice 2019
I took over as editor-in-chief of Heredity in July, 2016 but agreed to stay on for an additional term because of the Genetics Society Centenary in 2019. It has been an exciting year for the Genetics Society and it has been a pleasure to be involved. There have been Centenary events scattered throughout the year but highlights for me were: International Mendel day (see the paper by Daniel Fairbanks based on his presentation at this event); the Chelsea Flower Show (a particularly rewarding public engagement event because of genuine interest in genetics among gardeners); the Centenary birthday party at the John Innes Centre (with a particularly inspiring talk by Sir Paul Nurse, along with DNA cocktails and a commissioned song that set the tone for the dinner); and the Century of Genetics conference in Edinburgh (combining centenaries for both the Genetics Society and Animal Genetics at the Roslin Institute). We also published a fascinating special issue in Heredity, which featured personal perspectives from past presidents of the Genetics Society, put together by guest editor Allison Woollard.
We also are continuing to make changes at Heredity, to improve the author experience and to make sure that the journal is as relevant for the genetics community in its 72nd year as it was in its first. We have recently updated the remit and have added a new “computer notes” category; we have added an annual prize for best student paper; we have stopped charging for colour so publishing is now free unless authors choose gold open access; we are working with Springer Nature to make the initial submission process for authors easier, to develop a direct submission portal through BioRxiv, to improve social media presence, and take active measures to encourage open access publishing; we encourage authors to submit blogs as part of the Nature Ecology and Evolution Community. Our editorial assistant, Sandra Huettenbuegel, hired by the Genetics Society, provides a point of personal contact and ensures that the process is as efficient and author/reviewer friendly as possible.
The focus at Heredity is on quality rather than quantity and we aim to select papers for publication that will have broad appeal to the wide readership of the journal.
To highlight the breadth of focus of the journal and the expertise of our editorial team, I asked our Associate Editors to highlight papers that they handled in the past year. We have put together a web collection of these papers, with a commentary from the editors. We will also be featuring podcasts with our editors throughout the next year; you can hear the first interview with Alison Bentley here.
Barbara Mable
Editor-in-Chief, Heredity
Rowan Barrett
Recombination within the Cepaea nemoralis supergene is confounded by incomplete penetrance and epistasis
The shell colour and pattern system in Cepaea nemoralis is an iconic model for the study of polymorphism and ecological genetics in natural populations of animals. Classification into shell morph categories has been based on generally agreed categories backed up by breeding data, going back to early work by RA Fisher and Captain Cyril Diver in the 1930s. More recent investigations have shown that a ‘supergene’ containing tightly linked pigmentation loci is partially responsible for these shell morphs, but putative instances of recombination between loci within the supergene were difficult to verify. The paper by Davison et al. (Heredity 123, 153-161; 2019) applies a new set of C. nemoralis crosses and modern genetic methods to provide evidence for a lack of recombination between the main elements of a supergene, and shows that some anomalous results are most likely a consequence of variable penetrance and possibly epistasis, rather than recombination. The results are historically significant in that they cast doubt on the long-standing conclusions of a 1934 Nature correspondence between Fisher and Diver, and more generally the work suggests that more detailed investigation of the role of recombination in the architecture of supergenes may be warranted in other systems.
Alison Bentley
Heterotic patterns of primary and secondary metabolites in the oilseed crop Brassica juncea
Brassica juncea is an interesting mustard species used widely as a source of edible oil as well as an important source of food (as a leafy vegetable) and animal feed. Bajpai et al. (2019) reported metabolic analysis of F1 hybrids demonstrating that profiles in hybrids were distinct from their parents. Interestingly, the hybrids examined showed additive metabolite inheritance in reproductive tissue and this has potential application in breeding hybrids for seed quality traits such as oil production.
Armando Caballero
Genomic and phenotypic consequences of two independent secondary contact zones between allopatric lineages of the anadromous ice goby Leucopsarion petersii
Hirase and co-workers addressed the genomic and phenotypic consequences of two independent secondary contact zones of the ice goby, a small anadromous fish. Two varieties of this species living in the Japan sea and the Pacific Ocean are known that show partial isolation and genetic differentiation for several markers and quantitative traits. Hirase et al. (2019) characterised two secondary contact zones of these populations by using thousands of SNPs, mtDNA and several morphological traits, as well as carrying out a common garden experiment. They showed that in both contact zones there is an asymmetrical and enhanced introgression of mitochondrial genomes of either group relative to a little introgression of nuclear genomes, and that body size is regulated by non-neutral introgressed genes. The results give insight into the complexity of secondary contact zones.
Frank Hailer (Reviews Editor)
The population genetics of crypsis in vertebrates: recent insights from mice, hares, and lizards
One of the - arguably several - Holy Grails of evolutionary genetics is to identify the hereditary basis of positively selected phenotypic traits. Given the complex interplay of genetic drift and different types of selection, particularly well-understood case studies so far have investigated scenarios of strong selection. A key component of how (animal) species survive and adapt to their environment is how well they manage to avoid predation. Much work in evolutionary biology has therefore investigated the genetic and behavioural basis of predator avoidance.
In their fascinating review, Harris et al. (2020) discuss the population genetics of crypsis in vertebrates. The authors focus on cases where species avoid predation by concealing themselves through matching their colour to their surroundings and highlight how we can now apply theoretical predictions not just on individual sites/loci, but to entire genomic regions. Their reviewed examples of crypsis illustrate that the inference of selection from DNA sequence data first requires a robust understanding of past population demography. Only based on such approaches can we identify outlier genomic regions that have not evolved according to neutral expectations.
Particularly interesting for me was also the section of the review where Harris and colleagues discuss the role of dominance on the interplay of selection and migration, and how this can impact the extent and speed of local adaptation.
Jane Hughes
Hybridization drives genetic erosion in sympatric desert fishes of western North America
The paper by Chafin et al. (2019) uses modern genetic approaches to address some interesting questions about the potential effects of habitat modification on the maintenance or breakdown of species boundaries. ddRAD sequencing of two species of minnows is used to identify evidence for hybridization and introgression where the two species occur in sympatry. The implication is that areas of sympatry have occurred relatively recently as a result of a variety of human associated changes to the environment, bringing previously isolated species together. The idea is that where habitat has been modified, selection against interspecific heterozygotes breaks down. The results indicate that in one tributary, where the two species co-occur there was a hybrid swarm, while in another there was evidence of asymmetric introgression. Both of these would result in a loss of genetic integrity of the parental species.
I particularly liked the way the authors presented a nice mix of theory (ideas about reproductive isolation and maintenance of species boundaries) and management implications (concerning the conservation implications of anthropogenic habitat modification). The molecular methods used, ddRAD sequencing, and the analytical approaches employed, including genomic clines and analysis of first and second-generation hybrids, were innovative and presented clearly and their significance was well explained. The paper should therefore appeal to a broad audience that should include population geneticists, conservation ecologists and managers of freshwater habitats.
Pår Ingvarson
Genetic and genomic analysis of the seed-filling process in maize based on a logistic model
Seed filling is a complex trait involving a number of important biological processes (cell expansion, accumulation of proteins, oils, and carbohydrates) that have large effects on seed size and ultimately yield. Yin et al. (2020) studied seed filling in maize using a novel approach that involve dynamic modelling of the seed filling process. Fitting a logistic model to time course data on seed filling in a population of recombinant inbred lines allowed the authors to map several loci affecting this trait. A bulk-segregant RNAseq analysis was used to identify eight genes that show differential expression across the seed filling process and that also map to the QTL regions identified in the mapping population, including two loci implicated in starch and sucrose metabolism and the biosynthesis of secondary metabolites.
Louise Johnson
The fitness cost of mismatch repair mutators in Saccharomyces cerevisiae: partitioning the mutational load
The mismatch repair pathway corrects errors in DNA replication, so it is crucial for genome stability and strongly influences mutation rates. Galeota-Sprung et al. (2020) directly estimate, in yeast, the cost of mutational load in mismatch repair mutants. They use an unusual combination of techniques: the loads due to lethal and non-lethal mutation were estimated separately, the former using competition experiments and the latter by painstaking micromanipulation of mother and daughter yeast cells, respectively. Intriguingly, when the two types of load were combined, they explained the entire selective cost of these mismatch repair mutations. This has interesting implications for the evolution of mutation rates: if mismatch repair deficiencies bear only indirect costs – rather than having direct effects on individual growth rate – then the selective pressures on this pathway may depend sensitively on aspects of ecology such as mating system.
Sara Knott
Heritability of plumage colour morph variation in a wild population of promiscuous, long-lived Australian magpies
The paper by Dobson et al. (2019) was, on the surface, a relatively simple paper presenting the heritability of plumage colour in Australian magpies. On a closer read, however, the authors had to contend with a number of complicating factors making such studies rare in wild populations. First, recording the trait required trained observers. Second, the magpies are highly promiscuous and long-living, leading to difficulties in parentage assignment. A thorough analysis of the data was performed and the analyses and results clearly presented and discussed. The heritability was found to be very high, with little evidence for other influences. For me, however, the appeal of the paper was the overall feeling of a well thought through study with conscientious researchers - it was a pleasure to read.
Barbara Mable
Population structure in landrace barley (Hordeum vulgare L.) during the late 19th century crop failures in Fennoscandia
Of the 10 manuscripts that were ultimately accepted that I handled in 2019, particularly intriguing was one by Jenny Hagenblad and coauthors, from Linköping University, Sweden. They combined ancient DNA, deep sequencing, and novel statistical approaches to investigate origins and diversity of landraces of barley. The paper thus integrates all of the elements that form the core of Heredity: theory, state of the art molecular methods, historical context and application to an applied problem. The manuscript was also an “easy” one because the authors thoroughly addressed all comments from reviewers in a single round of revisions.
Marc Stift
The role of hybridisation in the origin and evolutionary persistence of vertebrate parthenogens: a case study of Darevskia lizards
I usually deal with papers about plants, but my editor´s highlight involves lizards (Freitas et al. 2019). For me, it stood out as an excellent example of how peer-review should function. Reviewers provided deep and constructive feedback. Authors revised and rebutted. This delayed publication, but ultimately led to a significantly improved paper. The result was well worth waiting for: an exciting, question-driven paper that challenges and develops fundamental hypotheses explaining the origin and persistence of asexual parthenogenic Darevskia lizards in sympatry with sexual taxa.
Bastiaan Star
Multiple interacting QTLs affect disease challenge survival in common carp (Cyprinus carpio)
Aquaculture is negatively affected by outbreaks of infectious diseases and solutions to these diseases are a huge challenge. The paper by Tadmor-Levi et al. (2019) investigates the genomic architecture underlying disease resistance in common carp. Carp aquaculture is very wide-spread, amongst the top 5 fish species produced in the world, and especially important for low income countries. The aim of this paper is to provide an understanding of the genomic basis of resistance to aid the breeding of such resistant strains to infectious diseases to provide a long-term, sustainable solution to outbreaks. What I find fascinating in this paper is that the authors have used feral strains as an unusual source of genetic variation to provide resistant phenotypes. Through WGS approaches, the authors then identify the genomic basis of resistance to disease in fish. What is particularly interesting is that they do find genes for resistance, but also identify this as a complex trait, which is not directly translated to different families of carp. Based on their findings, the authors come up with practical solutions to breeding of these species, which can greatly aid aquaculture without major economical investments.
Paul Sunnucks
Conservation genomic analysis reveals ancient introgression and declining levels of genetic diversity in Madagascar’s hibernating dwarf lemurs
The Williams et al. (2020) lemur paper was an excellent one. It uses sophisticated genomic approaches to answer questions that are of fundamental interest and relevant to understanding biodiversity. It was beautifully written and presented, and implemented advanced analyses.
Inbreeding load and inbreeding depression estimated from lifetime reproductive success in a small, dispersal-limited population
The Willoughby et al. (2019) banner-tailed kangaroo-rat one was a close second - also a great paper. The strength here was the combination of very long-term, in-depth field biology with strong analysis, resulting in important and yet rarely-obtained estimates of inbreeding depression on lifetime reproductive output and genetic load.
Jinliang Wang
Nearly unbiased estimator of contemporary effective mother size using within-cohort maternal sibling pairs incorporating parental and nonparental reproductive variations
Accelerated inbreeding depression suggests synergistic epistasis for deleterious mutations in Drosophila melanogaster
Bayesian model selection for the study of Hardy–Weinberg proportions and homogeneity of gender allele frequencies
Statistical power in genome-wide association studies and quantitative trait locus mapping
Analysis of trait heritability in functionally partitioned rice genomes
This year, Heredity has published several methodological papers in quantitative genetics and population genetics. Wang & Xu (2019) developed an analytical approach (as against the traditional simulation approach) to assess the power of a quantitative trait locus (QTL) study or a genome-wide association study (GWAS), which is useful for power analysis and experimental design. Puig et al. (2019) proposed a Bayesian method for the statistical test of Hardy–Weinberg equilibrium (HWE) in a population with possibly unequal allele frequencies in the two sexes, which broadens the traditional HWE tests. Akita (2019) developed a nearly unbiased estimator of effective mother size, based on a known maternal half-sibling relationship found within the same cohort. Heredity also published a study investigating the roles of nongenic and genic regions of the rice genome in determining the heritability of five agronomic traits (Wei et al. 2019), and a study revealing synergistic epistasis among deleterious alleles in an inbreeding experiment on Drosophila melanogaster (Domínguez-García et al. 2019).
Chenwu Xu
Genomic signatures of seed mass adaptation to global precipitation gradients in sorghum
Seed mass is a key component of adaptation in plants and a determinant of yield in crops. The climatic drivers and genomic basis of seed mass variation remain poorly understood. Wang et al. (2020) performed GWAS of seed mass and a genome scan of local adaptation, based on 1901 georeferenced and genotyped sorghum landraces, 100-seed mass estimates from common gardens and bioclimatic precipitation variables. They detected eleven a priori candidate seed size genes and eleven co-localized outlier SNPs, which were associated with seed mass and precipitation gradients. Their findings suggest that seed mass in sorghum was shaped by diversifying selection on drought stress, and can inform genomics-enabled breeding for climate-resilient cereals.
Yuan-Ming Zhang
Genome-wide association studies using binned genotypes
pKWmEB: integration of Kruskal–Wallis test with empirical Bayes under polygenic background control for multi-locus genome-wide association study
An expectation–maximization algorithm for the Lasso estimation of quantitative trait locus effects
pLARmEB: integration of least angle regression with empirical Bayes for multilocus genome-wide association studies
In genome-wide association studies, the number of markers is much more than sample size. Such big data faces high dimensionality problems in statistics. In this situation, dimension reduction is needed. I have highlighted several Heredity papers that have addressed this issue over the past decade. One approach is to select some potentially associated markers, by means of statistical methods, to reduce the high dimension marker space (Zhang et al. 2017; Ren et al. 2018). An alternative approach is to bin neighboring markers into a new synthetic marker (bin) without losing biological information, by means of linkage disequilibrium between neighboring markers, to resolve the above dilemma (An et al. 2019). Once the number of markers in multi-locus model is reduced to a manageable level, their effects can be estimated by penalized multiple regression methods, such as the least absolute shrinkage and selection operator (Xu 2010), and non-zero effects are further identified by likelihood ratio test for true QTN detection. In the big data era, all the above approaches are valuable in genome-wide association studies.
