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Rockman, M. V.

Publications and source records attributed to Rockman, M. V..

At least 19 recordsLinked to original sources

Caenorhabditis becei recombinant inbred lines (beRILs) reveal the scope of heritable variation within a gonochoristic nematode population.

Caenorhabditis nematodes are a powerful model clade for evolutionary genetics. Isogenic lines and panels of recombinant inbred lines (RILs) are among the most essential tools for genetic studies in these species. While most Caenorhabditis species are gonochoristic, large RIL panels have only been developed for self-fertilizing species. This gap biases our understanding and limits our ability to address questions related to the genetic architecture of traits in outbred populations, which have radically higher genetic diversity, heterozygosity, and effective recombination than selfers. Having previously identified Caenorhabditis becei as a tractable gonochoristic species due to its moderate inbreeding depression, we generated two panels of advanced-intercross RILs derived from three individual outbred C. becei worms collected from a single locality on Barro Colorado Island, Panama. One panel derives from a pair of worms sampled from a single rotting fig; the other derives from a cross between worms from two different figs. The panels share one founder in common, yielding two half-sib RIL panels. We sequenced and haplotyped the lines, identifying millions of variants and thousands of recombination breakpoints. Using simulations, we demonstrate the suitability of these lines for quantitative genetics studies and QTL mapping. In our single-fig panel, we observe abundant heritable variation in population growth rate, individual body size, and sexual dimorphism for body size. We detected four QTLs associated with population growth rate and show that estimated allelic effects are good predictors of selection that occurred during panel derivation.

genetics↗

Global genomic diversity of the selfing nematode Caenorhabditis tropicalis correlates with geography

Self-fertilization reduces genetic diversity compared to outcrossing and hypothetically decreases the ability to adapt to diverse environments. Among Caenorhabditis nematodes, self-fertilization evolved three times independently in Caenorhabditis elegans, Caenorhabditis briggsae, and the more recently discovered Caenorhabditis tropicalis. To survey C. tropicalis genetic relatedness, the influence of geography and niche on species-wide variation, and the signatures of selection, we collected 785 wild strains, sequenced their genomes, and identified 622 distinct genotypes (isotypes). In contrast to C. elegans and C. briggsae, C. tropicalis relatedness shows substantial association with geography and no transcontinental selective sweeps or broadly sampled isotypes. Populations from the Hawaiian Islands or Taiwan harbor more genetic variation than populations from the Caribbean or Americas, suggesting a Pacific species origin similar to other members of the Elegans subclade. Punctuated genomic regions of extreme genetic variation pervade the genome. These hyper-divergent regions (HDRs) comprise less than 6% of the reference genome in any given strain despite harboring 73% of all variant sites and are enriched for genes likely involved in environmental adaptation. HDRs represent a shared genomic feature of self-fertilizing Caenorhabditis nematodes despite their independent evolutionary origins and suggest a mechanism to explain worldwide distributions despite low species-wide levels of genetic variation.

genomics↗

Caenorhabditis briggsae ancestral genomic hyper-diversity contrasts with globally distributed genome-wide haplotypes

Comparative genomics provides a powerful framework to uncover the molecular and evolutionary mechanisms that shape genetic diversity within and across species, revealing how shared and lineage-specific processes influence their evolutionary trajectories through time. The nematode Caenorhabditis briggsae is distributed world-wide and is a comparative model to Caenorhabditis elegans in the biology of development, cellular mechanisms, neurobiology, genetic mappings of complex traits, and genome evolution. Following massive collection efforts by the nematode research community, we present the isolation of over 2,000 wild strains and analyses of genome sequences that catalog over six million single-nucleotide and insertion-deletion variants. This genome and strain resource provide a powerful means to interrogate the causal genetic bases of phenotypic variation for diverse traits. Additionally, we describe its global population structure and discover new and genetically distinct groups within this primarily self-fertilizing species, including groups of highly related strains that were sampled across different continents. We leverage expansive genetic variation to decipher the effects of linkage and selection on the distribution of genetic diversity across the genome and across geographic regions. Within the species, we find genomic regions with extremely high levels of genetic variation similar to hyper-divergent regions found in C. elegans and other species. These regions harbor new genes and variation enriched for environmental sensing and pathogen responses. In comparison to the outbreeding sister species Caenorhabditis nigoni, we conclude that long-term balancing selection has maintained substantial functional variation since the divergence from their outbreeding ancestor, likely in response to differences in the ecological niche. Overall, this massive strain resource enables future comparative genetics and genomics studies, including genome-wide association studies between Caenorhabditis species.

genomics↗

Natural variation suggests candidate genes underlying Caenorhabditis elegans susceptibility to diverse toxicants

Genetic differences among individuals shape how they respond to environmental toxicants, but the identification and validation of the genes responsible for this variation is difficult, particularly in humans. Consequently, our limited knowledge of the genes that influence susceptibility constrains our ability to accurately predict the risks posed by environmental toxicants. To identify genes underlying natural differences in toxicant susceptibilities, we measured the effects of 23 environmental toxicants on larval development across 195 genetically diverse Caenorhabditis elegans strains using a high-throughput imaging platform. We then combined these response data with whole-genome sequences to perform genome-wide association mappings, identifying 40 genomic regions where genetic variants are correlated with susceptibility differences. Many of these regions are enriched for genes involved in biological processes previously linked with toxicant responses, supporting the potential contributions of these genes to natural variation in susceptibility. Using a set of heuristics, we identified 94 candidate susceptibility genes, offering targets for experimental validation that could ultimately inform toxicant risk prediction and regulatory assessment by linking genetic variation to differences in susceptibility. Impact StatementAnalysis of natural genetic variation among 195 wild C. elegans strains identified 94 candidate genes putatively linked to differences in susceptibility to 23 environmental toxicants. These findings can inform the discovery of conserved susceptibility genes and the development of biomarkers that improve chemical risk assessment by accounting for genetic differences among humans.

pharmacology and toxicology↗

Caenorhabditis diversity on Pohnpei, Micronesia, provides evidence that the Elegans Supergroup has its roots in the Americas and diversified in the Pacific en route to Asia

The microscopic nematode Caenorhabditis elegans stands unrivaled as a model for developmental biology, neurobiology, and genetics, but fundamental aspects of its ecology, biogeography, and natural history remain unknown. Leveraging recent findings that place its center of diversity in the cool, high-elevation forests of Hawaii, we performed an intensive survey of the Caenorhabditis fauna of Pohnpei, a high island in Micronesia that is home to the largest patch of high-elevation forest between Hawaii and East Asia. We found nine species of Caenorhabditis, five of them new, but not C. elegans. Most species were limited to the hot lowlands but three spanned the elevational range and one was found only in the cloudforest. Using the distribution of Caenorhabditis nematodes among habitat patches - individual rotting fruits or flowers - we parameterized simple models that capture key aspects of the population biology of these animals. We generated transcriptomes for the new species and inferred a phylogeny for 70 species of Caenorhabditis, based on 2955 genes. This phylogeny allowed us to perform the first quantitative biogeographic analysis for the group. Our analysis suggests that the deep ancestors of the Elegans Supergroup of species lived in the Americas, and that the Supergroups subsequent diversification occurred in Remote Oceania. The ancestors of the Supergroup gave rise to a diverse Oceanian fauna and ultimately to multiple lineages that moved into Asia, Africa, Australasia, and back into the Americas. Though biogeographic inferences are limited by the lack of information from key regions of the southwest Pacific, the data are consistent with a model of trans-Pacific migration, with the islands of Oceania serving as sources rather than sinks for biodiversity.

evolutionary biology↗

Variation in inbreeding depression within and among Caenorhabditis species

Outbreeding populations harbor large numbers of recessive deleterious alleles that reduce the fitness of inbred individuals, and this inbreeding depression potentially shapes the evolution of mating systems, acting as a counterweight to the inherent selective advantage of self-fertilization. The population biological factors that influence inbreeding depression are numerous and often difficult to disentangle. We investigated the utility of obligately-outcrossing (gonochoristic) Caenorhabditis nematodes as models for inbreeding depression. By systematically inbreeding lines from ten populations and tracking line extinction, we found that inbreeding depression is universal but highly variable among species and populations. Inbreeding depression was detected across the life cycle, from mating to embryo production to embryonic viability and larval growth, and reciprocal crosses implicated female-biased effects. In most cases, the surviving inbred lines have dramatically reduced fitness, but the variance among inbred lines is substantial and compatible with the idea that inbreeding depression need not be an obstacle to the evolution of selfing in these worms. Populations of some species, including Caenorhabditis becei, exhibited modest inbreeding depression and could be tractable laboratory models for gonochoristic Caenorhabditis.

evolutionary biology↗

Five new Caenorhabditis species from Indonesia provide exceptions to Haldane's rule and partial fertility of interspecific hybrids

Given the interest in the biogeography and diversity of the Caenorhabditis genus, we established a collection of these nematodes from field surveys on four Indonesian islands. We isolated over 60 Caenorhabditis strains belonging to ten species. Five species were previously known from other locations: C. briggsae, which was predominant, C. tropicalis, C. nigoni, C. brenneri and C. elegans. The five other species are new, and we describe them here as Caenorhabditis indonesiana, Caenorhabditis malino, Caenorhabditis ceno, Caenorhabditis brawijaya and Caenorhabditis ubi. RNA sequence analysis of 1,861 orthologous genes placed all species from Indonesia in the Elegans group of Caenorhabditis species. Four of the new species belong to a Sinica subclade of species so far only found in an East Asia-Indo-Pacific world region. The fifth new species, C. indonesiana, appears as the sister of the C. tropicalis-C. wallacei pair, both also found in Indonesia. The present findings are thus consistent with diversification in the Elegans group having occurred in this world region. Crosses between closely related species showed counterexamples to Haldanes "rule": for two pairs of species, in one cross direction we only found hybrid males. In addition, we found a pair of species that could partially interbreed: Caenorhabditis ubi (East Java) with C. sp. 41 (Solomon islands), with the hybrid males in one cross direction being fertile. Such closesly related species pairs are good models for genetic studies of incompatibilities arising during speciation. SummaryThis work addresses their biodiversity, phylogenetic relationships and genetic incompatibilities of Caenorhabditis nematodes, which are laboratory model organisms. Through field studies, the authors isolated 60 Caenorhabditis strains in Indonesia, representing ten species, including five new. From RNA sequencing and phylogenetic reconstruction, all ten species belong to the Elegans group of Caenorhabditis. In crosses between closely related species, the hybrid progeny can be all females, abiding by Haldanes rule, but in other cases all males. In one species pair, partially fertile hybrids are produced in one cross direction. These closely related species are good models for studying genetic incompatibilities.

genetics↗

Conservative evolution of genetic and genomic features in Caenorhabditis becei, an experimentally tractable gonochoristic worm

Caenorhabditis nematodes represent a promising model clade for evolutionary genetics and genomics, but research has focused on the three androdioecious species, those with self-fertile hermaphrodites, all in the Elegans Group of species. The majority of Caenorhabditis species are gonochorists, with males and females, characterized by inconveniently high heterozygosity and inbreeding depression. We have identified C. becei as an experimentally tractable gonochorist. We show that transmission-genetic properties known from the androdioecious Elegans Group species are conserved in this Japonica Group species: the organization of the genetic map, cosegregation of autosomal indels and sex chromosomes, and segregation distortion due to Medea elements, demonstrated here for the first time in a gonochoristic Caenorhabditis species. We describe a new chromosomal genome assembly of a healthy inbred C. becei reference strain, integrating data from PacBio HiFi reads, Illumina short reads, genetic linkage, and HiC chromatin contacts, and experimental gene annotation with short- and long-read data. Some aspects of the genome are highly conserved, including synteny across the six chromosomes and the distributions of repetitive sequences and genes along each chromosome. Other features are quite distinctive, including evolved shifts in GC composition & heterogeneity along the genome. Both codon & amino acid usage are shifted in concert with the species' genomic GC content. C. becei has an unusually large X chromosome, which we find is associated with multiple local gene family expansions. These findings and resources lay the foundation for further experimental and computational studies of Caenorhabditis genetics and genomics.

evolutionary biology↗

Abundant Recurrent Mitochondrial Mutations and Widespread Mitonuclear Epistasis in Caenorhabditis elegans

Coordinated genetic and physical interactions between mitochondrial and nuclear gene products regulate ATP production in the mitochondria. Linking mitochondrial genotypes and mitonuclear genetic interactions to phenotypes remains a complex challenge. Here, we have developed Caenorhabditis elegans as a model for mitonuclear epistasis studies. In a sample of 540 genetically distinct wild isolates, 10% of sites in the mitochondrial genome vary, with hundreds of missense mutations segregating in the species. Recurrent mutations and triallelic sites are common. Phylogenetic analyses of mitogenome sequences identified eight distinct lineages, each with diagnostic variants. Principal component analysis of the nuclear genomes showed considerable concordance between mitochondrial and nuclear genomes in C. elegans populations, suggesting that disrupting coevolved mitonuclear genetic combinations could reveal substantial epistasis. We used GPR-1 overexpression, which disrupts the first mitotic division, to efficiently exchange nuclear and mitochondrial genomes between all pairs of 18 naturally isolated C. elegans strains, generating the largest-to-date animal mitonuclear exchange panel, with 323 unique viable mitonuclear genotypes. We phenotyped development of a subset of strains, with 30 unique genotypes, under six different environmental conditions, including high temperature and exposure to heavy metals. Mitonuclear epistasis contributed significantly to phenotypic variance across all tested conditions. We also tested for mitonuclear coadaptation by comparing the stress resistance of matched and mismatched cybrids. Interestingly, some mismatched strains exhibited greater resistance, highlighting the complexity and context dependence of mitonuclear interactions.

evolutionary biology↗

Parental-effect gene-drive elements under partial selfing, or why do Caenorhabditis genomes have hyperdivergent regions?

Self-fertile Caenorhabditis nematodes carry a surprising number of Medea elements, alleles that act in heterozygous mothers and cause death or developmental delay in offspring that dont inherit them. At some loci, both alleles in a cross operate as independent Medeas, affecting all the homozygous progeny of a selfing heterozygote. The genomic coincidence of Medea elements and ancient, deeply coalescing haplotypes, which pepper the otherwise homogeneous genomes of these animals, raises questions about how these apparent gene-drive elements persist for long periods of time. Here I investigate how mating system affects the evolution of Medeas, and their paternal-effect counterparts, peels. Despite an intuition that antagonistic alleles should induce balancing selection by killing homozygotes, models show that, under partial selfing, antagonistic elements experience positive frequency dependence: the common allele drives the rare one extinct, even if the rare one is more penetrant. Analytical results for the threshold frequency required for one allele to invade a population show that a very weakly penetrant allele, one whose effects would escape laboratory detection, could nevertheless prevent a much more penetrant allele from invading under high rates of selfing. Ubiquitous weak antagonistic Medeas and peels could then act as localized barriers to gene flow between populations, generating genomic islands of deep coalescence. Analysis of gene expression data, however, suggest that this cannot be the whole story. A complementary explanation is that ordinary ecological balancing selection generates ancient haplotypes on which Medeas can evolve, while high homozygosity in these selfers minimizes the role of gene drive in their evolution.

evolutionary biology↗

Sexual antagonism evolves when autosomes influence offspring sex ratio

Sex allocation theory generally assumes maternal control of offspring sex and makes few predictions for populations evolving under paternal control. Using population genetic simulations, we show that maternal and paternal control of the sex ratio lead to different equilibrium sex ratios in structured populations. Sex ratios evolved under paternal control are more female biased. This effect is dependent on the population subdivision; fewer founding individuals leads to both more biased sex ratios and a greater difference between the paternal and maternal equilibria. In addition, sexual antagonism evolves in simulations with both maternally- and paternally-acting loci. Maternally-acting loci continuously accumulate ever more female-biasing effects as male-biasing effects accumulate at paternally-acting loci. The difference in evolved sex-ratio equilibria and the evolution of sexual antagonism can be largely explained by differences in the between-group variance of maternal and paternal effects in the founding generation. These theoretical results apply to any system with biparental autosomal influence over offspring sex, opening up an exciting new line of questioning.

evolutionary biology↗

Environmental radiation exposure at Chornobyl has not systematically affected the genomes or mutagen tolerance phenotypes of local worms

The 1986 disaster at the Chornobyl Nuclear Power Plant transformed the surrounding region into the most radioactive landscape known on the planet. Questions remain regarding whether this sudden environmental shift selected for species, or even individuals within a species, that are naturally more resistant to radiation exposure. We collected, cultured, and cryopreserved 298 wild nematodes isolates from areas varying in radioactivity within the Chornobyl Exclusion Zone. We sequenced and assembled genomes de novo for 20 Oschieus tipulae strains, analyzed their genomes for evidence of recent mutation acquisition in the field and saw no evidence of an association between mutation and radiation level at the sites of collection. Multigenerational exposure of each of these strains to several mutagens in the lab revealed that strains vary heritably in tolerance to each mutagen, but mutagen tolerance cannot be predicted based on the radiation levels at collection sites.

genetics↗

Caenorhabditis nematodes colonize ephemeral resource patches in neotropical forests.

Factors shaping the distribution and abundance of species include life-history traits, population structure, and stochastic colonization-extinction dynamics. Field studies of model species groups help reveal the roles of these factors. Species of Caenorhabditis nematodes are highly divergent at the sequence level but exhibit highly conserved morphological uniformity, and many of these species live in sympatry on microbe-rich patches of rotten material. Here, we use field experiments and large-scale opportunistic collections to investigate species composition, abundance, and colonization efficiency of Caenorhabditis in two of the worlds best studied lowland tropical field sites: Barro Colorado Island in Panama and La Selva in Sarapiqui, Costa Rica. We observed seven species of Caenorhabditis, four of them known only from these collections. While these localities contain species from many parts of the phylogeny, both localities were dominated by globally distributed androdiecious species. We found that Caenorhabditis were able to colonize baits accessible only by phoresy, preferring to colonize baits making direct contact with the ground. We estimate founder numbers per colonization event to be low.

ecology↗

The genome of the poecilogonous annelid Streblospio benedicti

Streblospio benedicti is a common marine annelid that has become an important model for developmental evolution. It is the only known example of poecilogony, where two distinct developmental modes occur within a single species, that is due to a heritable difference in egg size. The dimorphic developmental programs and life-histories exhibited in this species depend on differences within the genome, making it an optimal model for understanding the genomic basis of developmental divergence. Studies using S. benedicti have begun to uncover the genetic and genomic principles that underlie developmental uncoupling, but until now they have been limited by the lack of availability of genomic tools. Here we present an annotated chromosomal-level genome assembly of S. benedicti generated from a combination of Illumina reads, Nanopore long reads, Chicago and Hi-C chromatin interaction sequencing, and a genetic map from experimental crosses. At 701.4 Mb, the S. benedicti genome is the largest annelid genome to date that has been assembled to chromosomal scaffolds, yet it does not show evidence of extensive gene family expansion, but rather longer intergenic regions. The complete genome of S. benedicti is valuable for functional genomic analyses of development and evolution, as well as phylogenetic comparison within the Annelida and the Lophotrochozoa. Despite having two developmental modes, there is no evidence of genome duplication or substantial gene number expansions. Instead, lineage specific repeats account for much of the expansion of this genome compared to other annelids.

genomics↗

Baby makes three: maternal, paternal, and zygotic genetic effects shape larval phenotypic evolution

The evolutionary potential of a population is shaped by the genetic architecture of its life-history traits. Early-life phenotypes are influenced by both maternal and offspring genotype, and efforts to understand life-history evolution therefore require consideration of the interactions between these separate but correlated genomes. We used a four-generation experimental pedigree to estimate the genetic architecture of early-life phenotypes in a species with dramatic variation in larval size and morphology. In the polychaete annelid Streblospio benedicti, females make either many small eggs that develop into complex larvae that feed in the plankton or few large eggs that develop into benthic juveniles without having to feed as larvae. By isolating the contributions of maternal, paternal, and zygotic genotype to larval traits, we determined that larval anatomical structures are governed by the offspring genotype at a small number of large-effect loci. Larval size is not shaped by the larvas own genotype but instead depends on loci that act in the mother, and at two genomic locations, by loci that act in the father. The overall phenotype of each larva thus depends on three separate genomes, and a populations response to selection on larval traits will reflect the interactions among them.

evolutionary biology↗

Selfing is the safest sex for Caenorhabditis tropicalis

Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, C. tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple gene drive elements, genetically consistent with maternal toxin/zygotic antidote systems. Driver loci harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating drivers dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid drive-mediated outbreeding depression.

evolutionary biology↗

Gene-level quantitative trait mapping in an expanded C. elegans multiparent experimental evolution panel

The Caenorhabditis elegans multiparental experimental evolution (CeMEE) panel is a collection of genome-sequenced, cryopreserved recombinant inbred lines useful for mapping the genetic basis and evolution of quantitative traits. We have expanded the resource with new lines and new populations, and here report updated additive and epistatic mapping simulations and the genetic and haplotypic composition of CeMEE version 2. Additive QTL explaining 3% of trait variance are detected with >80% power, and the median detection interval is around the length of a single gene on the highly recombinant chromosome arms. Although CeMEE populations are derived from a long-term evolution experiment, genetic structure is dominated by variation present in the ancestral population and is not obviously associated with phenotypic differentiation. C. elegans provides exceptional experimental advantages for the study of phenotypic evolution.

evolutionary biology↗

Cryptic asexual reproduction in Caenorhabditis nematodes revealed by interspecies hybridization

Although most unicellular organisms reproduce asexually, most multicellular eukaryotes are obligately sexual. This implies that there are strong barriers that prevent the origin or maintenance of asexuality arising from an obligately sexual ancestor. By studying rare asexual animal species we can gain a better understanding of the circumstances that facilitate their evolution from a sexual ancestor. Of the known asexual animal species, many originated by hybridization between two ancestral sexual species. The balance hypothesis predicts that genetic incompatibilities between the divergent genomes in hybrids can modify meiosis and facilitate asexual reproduction, but there are few instances where this has been shown. Here we report that hybridizing two sexual Caenorhabditis nematode species (C. nouraguensis females and C. becei males) alters the normal inheritance of the maternal and paternal genomes during the formation of hybrid zygotes. Most offspring of this interspecies cross die during embryogenesis, exhibiting inheritance of a diploid C. nouraguensis maternal genome and incomplete inheritance of C. becei paternal DNA. However, a small fraction of offspring develop into viable adults that can be either fertile or sterile. Fertile offspring are produced asexually by sperm-dependent parthenogenesis (also called gynogenesis or pseudogamy); these progeny inherit a diploid maternal genome but fail to inherit a paternal genome. Sterile offspring are hybrids that inherit both a diploid maternal genome and a haploid paternal genome. Whole-genome sequencing of individual viable worms shows that diploid maternal inheritance in both fertile and sterile offspring results from an altered meiosis in C. nouraguensis oocytes and the inheritance of two randomly selected homologous chromatids. We hypothesize that hybrid incompatibility between C. nouraguensis and C. becei modifies maternal and paternal genome inheritance and indirectly induces gynogenetic reproduction. This system can be used to dissect the molecular mechanisms by which hybrid incompatibilities can facilitate the emergence of asexual reproduction. AUTHOR SUMMARYEukaryotes employ two major reproductive strategies: sexual and asexual reproduction. Both types of reproduction have distinct theoretical costs and benefits, and most unicellular eukaryotes can switch between both modes. However, most multicellular eukaryotes are obligately sexual, implying that there are barriers to the evolution of asexuality from a sexual ancestor. Of the few asexual animal species, many are hybrids of two ancestral sexual species, suggesting that novel genetic interactions in hybrids facilitate the evolution of asexuality. One model suggests that genetic incompatibilities between divergent genomes in hybrids can modify female meiosis and paternal genome inheritance to facilitate asexual reproduction. While studying interspecies hybridizations of Caenorhabditis nematodes, we found that crossing two sexual species (C. nouraguensis and C. becei) disrupts female meiosis and paternal genome inheritance. Most offspring die during embryogenesis, but on rare occasions develop into viable and fertile adults that are produced asexually. This asexual reproduction involves the unusual production of eggs carrying two sets of maternal chromosomes and the loss of the paternal set of chromosomes. We hypothesize that genetic incompatibility between these two species disrupts maternal and paternal genome inheritance. This interspecies hybridization may serve as a model to study how genetic incompatibilities facilitate the emergence of asexuality.

evolutionary biology↗