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Caenorhabditis nematodes form an excellent model for studying how the mode of reproduction affects genetic diversity, as some species reproduce via outcrossing whereas others can self-fertilize. Currently, chromosome-level patterns of diversity and recombination are only available for self-reproducing Caenorhabditis, making the generality of genomic patterns across the genus unclear given the profound potential influence of reproductive mode. Here we present a whole-genome diversity landscape, coupled with a new genetic map, for the outcrossing nematode C. remanei. We demonstrate that the genomic distribution of recombination in C. remanei, like the model nematode C. elegans, shows high recombination rates on chromosome arms and low rates toward the central regions. Patterns of genetic variation across the genome are also similar between these species, but differ dramatically in scale, being tenfold greater for C. remanei. Historical reconstructions of variation in effective population size over the past million generations echo this difference in polymorphism. Evolutionary simulations demonstrate how selection, recombination, mutation, and selfing shape variation along the genome, and that multiple drivers can produce patterns similar to those observed in natural populations. The results illustrate how genome organization and selection play a crucial role in shaping the genomic pattern of diversity whereas demographic processes scale the level of diversity across the genome as a whole. Author summary: The mode of reproductive exchange among individuals has a profound effect on genetic diversity. In self-reproducing organisms, absence of genetic interchange between individuals reduces the effective population size and increases linkage among segregating sites at different genes, leading to lower diversity than outcrossing species. Caenorhabditis nematodes offer an exceptional system for studying the genomic effects of different systems of mating. While selfing species such as C. elegans have been studied, we present the first recombination map and genome-wide landscape of polymorphism for an outcrossing member of the genus, C. remanei. We find that, similar to C. elegans, C. remanei has high recombination rates on chromosome arms and low rates in central regions. The genomic diversity landscapes of these species are qualitatively similar, with higher diversity in the regions of higher recombination. However, C. remanei exhibits tenfold greater diversity than C. elegans due to their much larger effective population size and the decreased impact of linked selection as an outcrossing species. We use evolutionary simulations to show the influence of genomic and demographic processes work on these patterns. This work illustrates how understanding complex interactions among genetics, genomics, and reproduction is fundamental to describing patterns of genetic variation within natural populations. [ABSTRACT FROM AUTHOR]

Males of Caenorhabditis elegans provide a crucial practical tool in the laboratory, but, as the rarer and more finicky sex, have not enjoyed the same depth of research attention as hermaphrodites. Males, however, have attracted the attention of evolutionary biologists who are exploiting the C. elegans system to test longstanding hypotheses about sexual selection, sexual conflict, transitions in reproductive mode, and genome evolution, as well as to make new discoveries about Caenorhabditis organismal biology. Here, we review the evolutionary concepts and data informed by study of males of C. elegans and other Caenorhabditis. We give special attention to the important role of sperm cells as a mediator of inter-male competition and male-female conflict that has led to drastic trait divergence across species, despite exceptional phenotypic conservation in many other morphological features. We discuss the evolutionary forces important in the origins of reproductive mode transitions from males being common (gonochorism: females and males) to rare (androdioecy: hermaphrodites and males) and the factors that modulate male frequency in extant androdioecious populations, including the potential influence of selective interference, host-pathogen coevolution, and mutation accumulation. Further, we summarize the consequences of males being common vs rare for adaptation and for trait divergence, trait degradation, and trait dimorphism between the sexes, as well as for molecular evolution of the genome, at both micro-evolutionary and macro-evolutionary timescales.We conclude that C. elegans male biology remains underexploited and that future studies leveraging its extensive experimental resources are poised to discover novel biology and to inform profound questions about animal function and evolution. [ABSTRACT FROM AUTHOR]

Deciphering the genetic and developmental causes of the disproportionate rarity, inviability, and sterility of hybrid males, Haldane's rule, is important for understanding the evolution of reproductive isolation between species. Moreover, extrinsic and prezygotic factors can contribute to the magnitude of intrinsic isolation experienced between species with partial reproductive compatibility. Here, we use the nematodes Caenorhabditis briggsae and C. nigoni to quantify the sensitivity of hybrid male viability to extrinsic temperature and developmental timing, and test for a role of mito-nuclear incompatibility as a genetic cause. We demonstrate that hybrid male inviability manifests almost entirely as embryonic, not larval, arrest and is maximal at the lowest rearing temperatures, indicating an intrinsic-by-extrinsic interaction to hybrid inviability. Crosses using mitochondrial substitution strains that have reciprocally introgressed mitochondrial and nuclear genomes show that mito-nuclear incompatibility is not a dominant contributor to postzygotic isolation and does not drive Haldane's rule in this system. Crosses also reveal that competitive superiority of X-bearing sperm provides a novel means by which postmating prezygotic factors exacerbate the rarity of hybrid males. These findings highlight the important roles of gametic, developmental, and extrinsic factors in modulating the manifestation of Haldane's rule. [ABSTRACT FROM AUTHOR]

Sperm from other species invade female tissues to cause sterility and death, helping to keep nematode species boundaries intact. [ABSTRACT FROM AUTHOR]

The rapid pace of species discovery outstrips the rate of species description in many taxa. This problem is especially acute for Caenorhabditis nematodes, where the naming of distinct species would greatly improve their visibility and usage for biological research, given the thousands of scientists studying Caenorhabditis. Species description and naming has been hampered in Caenorhabditis, in part due to the presence of morphologically cryptic species despite complete biological reproductive isolation and often enormous molecular divergence. With the aim of expediting species designations, here we propose and apply a revised framework for species diagnosis and description in this group. Our solution prioritizes reproductive isolation over traditional morphological characters as the key feature in delineating and diagnosing new species, reflecting both practical considerations and conceptual justifications. DNA sequence divergence criteria help prioritize crosses for establishing patterns of reproductive isolation among the many species of Caenorhabditis known to science, such as with the ribosomal internal transcribed spacer-2 (ITS2) DNA barcode. By adopting this approach, we provide new species name designations for 15 distinct biological species, thus increasing the number of named Caenorhabditis species in laboratory culture by nearly 3-fold. We anticipate that the improved accessibility of these species to the research community will expand the opportunities for study and accelerate our understanding of diverse biological phenomena. [ABSTRACT FROM AUTHOR]

The biology of Sydney Brenner's eponymous species of nematode, Caenorhabditis brenneri, is little known to science, despite its famous sibling Caenorhabditis elegans. Here we demonstrate that C brenneri harbors the most molecular diversity of any eukaryote, with its 14.1% of polymorphic synonymous sites between individuals being 150-fold greater than humans and most comparable to hyperdiverse bacteria. This diversity is not an artifact of cryptic species divergence but reflects an enormous pan-tropical population, confirmed by fully viable genetic crosses between continents, extensive intralocus recombination, selection on codon use, and only weak geographic genetic structure. These findings in an animal galvanize tests of theory about the evolution of complexity in genomes and phenotypes and enable molecular population genetics methods to finely resolve uncharacterized functional noncoding elements. [ABSTRACT FROM AUTHOR]

Temperature-dependent behaviours in Caenorhabditis elegans, such as thermotaxis and isothermal tracking, are complex behavioural responses that integrate sensation, foraging and learning, and have driven investigations to discover many essential genetic and neural pathways. The ease of manipulation of the Caenorhabditis model system also has encouraged its application to comparative analyses of phenotypic evolution, particularly contrasts of the classic model C. elegans with C. briggsae. And yet few studies have investigated natural genetic variation in behaviour in any nematode. Here we measure thermotaxis and isothermal tracking behaviour in genetically distinct strains of C. briggsae, further motivated by the latitudinal differentiation in C. briggsae that is associated with temperature-dependent fitness differences in this species. We demonstrate that C. briggsae performs thermotaxis and isothermal tracking largely similar to that of C. elegans, with a tendency to prefer its rearing temperature. Comparisons of these behaviours among strains reveal substantial heritable natural variation within each species that corresponds to three general patterns of behavioural response. However, intraspecific genetic differences in thermal behaviour often exceed interspecific differences. These patterns of temperature-dependent behaviour motivate further development of C. briggsae as a model system for dissecting the genetic underpinnings of complex behavioural traits. [ABSTRACT FROM AUTHOR]

Background: In stark contrast to the wealth of detail about C. elegans developmental biology and molecular genetics, biologists lack basic data for understanding the abundance and distribution of Caenorhabditis species in natural areas that are unperturbed by human influence. Methods: Here we report the analysis of dense sampling from a small, remote site in the Amazonian rain forest of the Nouragues Natural Reserve in French Guiana. Results: Sampling of rotting fruits and flowers revealed proliferating populations of Caenorhabditis, with up to three different species co-occurring within a single substrate sample, indicating remarkable overlap of local microhabitats. We isolated six species, representing the highest local species richness for Caenorhabditis encountered to date, including both tropically cosmopolitan and geographically restricted species not previously isolated elsewhere. We also documented the structure of within-species molecular diversity at multiple spatial scales, focusing on 57 C. briggsae isolates from French Guiana. Two distinct genetic subgroups co-occur even within a single fruit. However, the structure of C. briggsae population genetic diversity in French Guiana does not result from strong local patterning but instead presents a microcosm of global patterns of differentiation. We further integrate our observations with new data from nearly 50 additional recently collected C. briggsae isolates from both tropical and temperate regions of the world to re-evaluate local and global patterns of intraspecific diversity, providing the most comprehensive analysis to date for C. briggsae population structure across multiple spatial scales. Conclusions: The abundance and species richness of Caenorhabditis nematodes is high in a Neotropical rainforest habitat that is subject to minimal human interference. Microhabitat preferences overlap for different local species, although global distributions include both cosmopolitan and geographically restricted groups. Local samples for the cosmopolitan C. briggsae mirror its pan-tropical patterns of intraspecific polymorphism. It remains an important challenge to decipher what drives Caenorhabditis distributions and diversity within and between species. [ABSTRACT FROM AUTHOR]

Mounting evidence points to differences in gene regulation as a major source of phenotypic variation. MicroRNA-mediated post-transcriptional regulation has emerged recently as a key factor controlling gene activity during development. MicroRNA genes are abundant in genomes, acting as managers of gene expression by directing translational repression. Thus, understanding the role of microRNA sequence variation within populations is essential for fully dissecting the origin and maintenance of phenotypic diversity in nature. In this study, we investigate allelic variation at microRNA loci in the nematode Caenorhabditis briggsae, a close relative of C. elegans. Phylogeographic structure in C. briggsae partitions most strains from around the globe into a "temperate" or a "tropical" clade, with a few strains having divergent, geographically restricted genotypes. Remarkably, strains that follow this latitudinal dichotomy also differ in temperature-associated fitness. With this phylogeographic pattern in mind, we examined polymorphisms in 18 miRNAs in a global sample of C. briggsae isolates and tested whether newly isolated strains conform to this phylogeography. Surprisingly, nucleotide diversity is relatively high in this class of gene that generally experiences strong purifying selection. In particular, we find that miRNAs in C. briggsae are substantially more polymorphic than in Arabidopsis thaliana, despite similar background levels of neutral site diversity between the two species. We find that some mutations suggest functional divergence on the basis of requirements for target site recognition and computational prediction of the effects of the polymorphisms on RNA folding. These findings demonstrate the potential for miRNA polymorphisms to contribute to phenotypic variation within a species. Sequences were deposited in GenBank under accession nos. JN251323--JN251744. [ABSTRACT FROM AUTHOR]

New genomic resources and genetic tools of the past few years have advanced the nematode genus Caenorhabditis as a model for comparative biology. However, understanding of natural genetic variation at molecular and phenotypic levels remains rudimentary for most species in this genus, and for C. briggsae in particular. Here we characterize phenotypic variation in C. briggsae’s sensitivity to the potentially important and variable environmental toxin, ethanol, for globally diverse strains. We also quantify nucleotide variation in a new sample of 32 strains from four continents, including small islands, and for the closest-known relative of this species ( C. sp. 9). We demonstrate that C. briggsae exhibits little heritable variation for the effects of ethanol on the norm of reaction for survival and reproduction. Moreover, C. briggsae does not differ significantly from C. elegans in our assays of its response to this substance that both species likely encounter regularly in habitats of rotting fruit and vegetation. However, we uncover drastically more molecular genetic variation than was known previously for this species, despite most strains, including all island strains, conforming to the broad biogeographic patterns described previously. Using patterns of sequence divergence between populations and between species, we estimate that the self-fertilizing mode of reproduction by hermaphrodites in C. briggsae likely evolved sometime between 0.9 and 10 million generations ago. These insights into C. briggsae’s natural history and natural genetic variation greatly expand the potential of this organism as an emerging model for studies in molecular and quantitative genetics, the evolution of development, and ecological genetics. [ABSTRACT FROM AUTHOR]

The nematode Caenorhabditis elegans reproduces primarily by self-fertilization of hermaphrodites, yet males are present at low frequencies in natural populations (androdioecy). The ancestral state of C. elegans was probably gonochorism (separate males and females), as in its relative C. remanei. Males may be maintained in C. elegans because outcrossed individuals escape inbreeding depression. The level of inbreeding depression is, however, expected to be low in such a highly selfing species, compared with an outcrosser like C. remanei. To investigate these issues, we measured life-history traits in the progeny of inbred versus outcrossed C. elegans and C. remanei individuals derived from recently isolated natural populations. In addition, we maintained inbred lines of C. remanei through 13 generations of full-sibling mating. Highly inbred C. remanei showed dramatic reductions in brood size and relative fitness compared to outcrossed individuals, with evidence of both direct genetic and maternal-effect inbreeding depression. This decline in fitness accumulated over time, causing extinction of nearly 90% of inbred lines, with no evidence of purging of deleterious mutations from the remaining lines. In contrast, pure strains of C. elegans performed better than crosses between strains, indicating outbreeding depression. The results are discussed in relation to the evolution of androdioecy and the effect of mating system on the level of inbreeding depression. [ABSTRACT FROM AUTHOR]

The common ancestor of the self-fertilizing nematodes Caenorhabditis elegans and C. briggsae must have reproduced by obligate outcrossing, like most species in this genus. However, we have only a limited understanding about how genetic variation is patterned in such male-female (gonochoristic) Caenorhabditis species. Here, we report results from surveying nucleotide variation of six nuclear loci in a broad geographic sample of wild isolates of the gonochoristic C. remanei. We find high levels of diversity in this species, with silent-site diversity averaging 4.7%, implying an effective population size close to ~ million. Additionally, the pattern of polymorphisms reveals little evidence for population structure or deviation from neutral expectations, suggesting that the sampled C. remanei populations approximate panmixis and demographic equilibrium. Combined with the observation that linkage disequilibrium between pairs of polymorphic sites decays rapidly with distance, this suggests that C. remanei will provide an excellent system for identifying the genetic targets of natural selection from deviant patterns of polymorphism and linkage disequilibrium. The patterns revealed in this obligately outcrossing species may provide a useful model of the evolutionary circumstances in C. elegans' gonochoristic progenitor. This will be especially important if self-fertilization evolved recently in C. elegans history, because most of the evolutionary time separating C. elegans from its known relatives would have occurred in a state of obligate outcrossing. [ABSTRACT FROM AUTHOR]

Caenorhabditis briggsae provides a natural comparison species for the model nematode C. elegans, given their similar morphology, life history, and hermaphroditic mode of reproduction. Despite C. briggsae boasting a published genome sequence and establishing Caenorhabditis as a model genus for genetics and development, little is known about genetic variation across the geographic range of this species. In this study, we greatly expand the collection of natural isolates and characterize patterns of nucleotide variation for six loci in 63 strains from three continents. The pattern of polymorphisms reveals differentiation between C. briggsae strains found in temperate localities in the northern hemisphere from those sampled near the Tropic of Cancer, with diversity within the tropical region comparable to what is found for C. elegans in Europe. As in C. elegans, linkage disequilibrium is pervasive, although recombination is evident among some variant sites, indicating that outcrossing has occurred at a low rate in the history of the sample. In contrast to C. elegans, temperate regions harbor extremely little variation, perhaps reflecting colonization and recent expansion of C. briggsae into northern latitudes. We discuss these findings in relation to their implications for selection, demographic history, and the persistence of self-fertilization. [ABSTRACT FROM AUTHOR]

Background: Reproductive interference can mediate interference competition between species through sexual interactions that reduce the fitness of one species by another. Theory shows that the positive frequency-dependent effects of such costly errors in mate recognition can dictate species coexistence or exclusion even with countervailing resource competition differences between species. While usually framed in terms of pre-mating or post-zygotic costs, reproductive interference manifests between individual Caenorhabditis nematodes from negative interspecies gametic interactions: sperm cells from interspecies matings can migrate ectopically to induce female sterility and premature death. The potential for reproductive interference to exert population level effects on Caenorhabditis trait evolution and community structure, however, remains unknown. Results: Here we test whether a species that is superior in individual-level reproductive interference (C. nigoni) can exact negative demographic effects on competitor species that are superior in resource competition (C. briggsae and C. elegans). We observe coexistence over six generations and find evidence of demographic reproductive interference even under conditions unfavorable to its influence. C. briggsae and C. elegans show distinct patterns of reproductive interference in competitive interactions with C. nigoni. Conclusions: These results affirm that individual level negative effects of reproductive interference mediated by gamete interactions can ramify to population demography, with the potential to influence patterns of species coexistence separately from the effects of direct resource competition. [ABSTRACT FROM AUTHOR]

A correction to the article "Reproductive Mode and the Evolution of Genome Size and Structure in Caenorhabditis Nematodes" is presented.

Species with broad ecological amplitudes with respect to a key focal resource, niche generalists, should maintain larger and more connected populations than niche specialists, leading to the prediction that nucleotide diversity will be lower and more subdivided in specialists relative to their generalist relatives. This logic describes the specialist-generalist variation hypothesis (SGVH). Some outbreeding species of Caenorhabditis nematodes use a variety of invertebrate dispersal vectors and have high molecular diversity. By contrast, Caenorhabditis japonica lives in a strict association and synchronized life cycle with its dispersal host, the shield bug Parastrachia japonensis, itself a diet specialist. Here, we characterize sequence variation for 20 nuclear loci to investigate how C. japonica's life history shapes nucleotide diversity. We find that C. japonica has more than threefold lower polymorphism than other outbreeding Caenorhabditis species, but that local populations are not genetically disconnected. Coupled with its restricted range, we propose that its specialist host association contributes to a smaller effective population size and lower genetic variation than host generalist Caenorhabditis species with outbreeding reproductive modes. A literature survey of diverse organisms provides broader support for the SGVH. These findings encourage further testing of ecological and evolutionary hypotheses with comparative population genetics in Caenorhabditis and other taxa. [ABSTRACT FROM AUTHOR]

The combined actions of natural selection, mutation, and recombination forge the landscape of genetic variation across genomes. One frequently observed manifestation of these processes is a positive association between neutral genetic variation and local recombination rates. Two selective mechanisms and/or recombination-associated mutation (RAM) could generate this pattern, and the relative importance of these alternative possibilities remains unresolved generally. Here we quantify nucleotide differences within populations, between populations, and between species to test for genome-wide effects of selection and RAM in the partially selfing nematode Caenorhabditis briggsae. We find that nearly half of genome-wide variation in nucleotide polymorphism is explained by differences in local recombination rates. By quantifying divergence between several reproductively isolated lineages, we demonstrate that ancestral polymorphism generates a spurious signal of RAM for closely related lineages, with implications for analyses of humans and primates; RAM is, at most, a minor factor in C. briggsae. We conclude that the positive relation between nucleotide polymorphism and the rate of crossover represents the footprint of natural selection across the C. briggsae genome and demonstrate that background selection against deleterious mutations is sufficient to explain this pattern. Hill-Robertson interference also leaves a signature of more effective purifying selection in high-recombination regions of the genome. Finally, we identify an emerging contrast between widespread adaptive hitchhiking effects in species with large outcrossing populations (e.g., Drosophila) versus pervasive background selection effects on the genomes of organisms with self-fertilizing lifestyles and/or small population sizes (e.g., Caenorhabditis elegans, C. briggsae, Arabidopsis thaliana, Lycopersicon, human). These results illustrate how recombination, mutation, selection, and population history interact in important ways to shape molecular heterogeneity within and between genomes. [ABSTRACT FROM AUTHOR]

Summary: In the nematode Caenorhabditis elegans, a single gene (plg-1) encodes the dominant protein found in mating plugs — a means of inhibiting multiple matings. Naturally occurring loss of plg-1 function results in males that fail to deposit mating plugs — a manifestation of relaxed sexual selection since the evolution of self-fertilization in this species. [Copyright &y& Elsevier]