Species richness, distribution and genetic diversity of Caenorhabditis nematodes in a remote tropical rainforest
- Marie-Anne Félix†1,
- Richard Jovelin†2,
- Céline Ferrari3, 4, 5,
- Shery Han2,
- Young Ran Cho2,
- Erik C Andersen6,
- Asher D Cutter2 and
- Christian Braendle3, 4, 5Email author
© Félix et al.; licensee BioMed Central Ltd. 2013
Received: 9 October 2012
Accepted: 7 January 2013
Published: 12 January 2013
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.
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.
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.
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.
KeywordsCaenorhabditis Species richness Population structure C. briggsae Nucleotide diversity
Understanding the patterns and drivers that govern the abundance and diversity of organisms motivates the study of ecology and evolution. Historically, however, such study has focused primarily on non-model organisms, with some notable exceptions (e.g. Drosophila melanogaster in evolutionary biology). Ecological and evolutionary investigations have particularly neglected the nematode Caenorhabditis elegans and its close relatives until recently [1, 2]. And yet, the deep mechanistic knowledge about C. elegans development and life history, coupled with its experimental advantages in the laboratory, make it particularly suited for a more complete integration of molecular genetic approaches with evolutionary and ecological questions. This merging of disciplines is motivated further by interesting phylogenetically variable characteristics of the genus, such as the independent origins of androdioecy (i.e. self-fertilizing reproduction by hermaphrodites and facultative outcrossing with males) in at least three lineages from the more prevalent gonochoristic reproductive mode among other Caenorhabditis species, which reproduce through obligatory mating of females and males [3, 4]. A major impediment to fully realizing the potential of integrating these fields, however, is the lack of basic information about species distribution and richness in nature.
Studies of Caenorhabditis in nature are difficult, not only because of their small size (ca. 1 mm length), but also because we know little about the habitats in which they can be found reliably . For this reason, the first population genetic analyses on C. elegans were conducted from opportunistic collection or by sampling populations in artificial compost heaps [5–10]. Subsequently, C. elegans was isolated from rotting fruits, as well as in phoretic association with invertebrates such as snails, slugs and isopods [3, 5, 11, 12]. Compost heap populations are mostly composed of animals in dauer diapause, but C. elegans and C. briggsae were recently shown to proliferate and feed in rotting fruits and stems in mainland France . Those rotting fruits were collected primarily in human-built orchards; although rotting stems are found in natural preserves, primary forests no longer exist in Europe . Like many other model organisms (Drosophila melanogaster, Saccharomyces cerevisiae, Mus musculus), C. elegans is thus at least partly human-associated, which likely exerts a strong influence on its range, migration patterns, and population structure [5, 14, 15]. However, we still have very limited information on the distribution of C. elegans and other Caenorhabditis species relating to habitat type and geographic location. Most importantly, we lack information on Caenorhabditis species diversity and population structure from unperturbed habitats.
Here, we report the results of a systematic sampling of Caenorhabditis across spatial scales, from within a single fruit to sampling at metre, kilometre, regional and global scales. In order to minimize the impact of humans and to contrast previously studied temperate sites with a tropical location, we sampled Caenorhabditis populations in a primary Neotropical rain forest in French Guiana, at the Nouragues National Reserve. We quantified the structure of diversity at different genetic and spatial scales, including the species richness of Caenorhabditis at the Nouragues location. In addition, we examined levels of intraspecific molecular polymorphism of C. briggsae from French Guiana and from additional recent local sampling of C. briggsae from different regions of the world.
Species diversity in French Guiana
Summary of Caenorhabditis species and isolates isolated from different localities in French Guiana
Mode of reproduction*
Number of isolates
Locations in French Guiana (No. of isolates)
Nouragues (54), Montagne des Singes (6), Montabo (1), Petit Saut (1)
C. sp. 11
Nouragues (30), Kaw mountain (1)
Nouragues (9), Montabo (1), Comté riverbank (1), Cacao (2)
C. sp. 17
Nouragues (28), Montagne des Singes (2)
C. sp. 18
C. sp. 12
Substrate type and presence of Caenorhabditis
We found Caenorhabditis nematodes in a wide variety of rotting vegetal substrates (fruits, flowers, plant stems); however, we could not detect any obvious substrate specificity of the different species (Additional file 2). Samples examined immediately after isolation indicated that Caenorhabditis population size in a given sample varied greatly, from one to approximately one thousand individuals, including both dauer stages and proliferating populations with non-dauer juvenile and adult stages (Additional file 2). Of the 130 Nouragues samples, 33 (25%) contained Caenorhabditis, including 16 of 48 rotting fruits and 11 of 19 rotting flowers. Proliferating populations of Caenorhabditis were found both in rotting fruits and flowers, as well as in one of three samples of erect live flowers (Heliconia sp.). Caenorhabditis nematodes were rarely found in humus or leaf litter (3 of 24) or in association with live or dead insects (0 of ~20). In 8 of 33 positive samples, we found two or three different Caenorhabditis species co-occurring in rotting fruits or flowers sampled at the same site (e.g. C. briggsae, spp. 11 and 17, isolated from Cecropia fruits, sample D25, Additional file 2). Many samples also contained nematode species other than Caenorhabditis, including members of the Rhabditina (e.g. Oscheius spp.), Diplogastrina or Aphelenchida.
Distribution of Caenorhabditisspecies at different spatial scales
Pattern of C. briggsaegenetic diversity at different spatial scales
To test for local population structure within a species, we focused on the C. briggsae isolates resulting from the above small-scale spatial analysis, then considered these together with isolates from the entire Nouragues area and from other sampling sites in French Guiana. We further placed the results in the context of worldwide diversity of this species.
Differentiation ( F ST , below diagonal) and per-site divergence ( D xy , above diagonal) between phylogeographic groups for the 6 nuclear loci combined
Tropical/I (n = 97)
Temperate/II (n = 76)
Nairobi (n = 8)
Kerala* (n = 3)
Taiwan* (n = 2)
Montreal (n = 2)
The genetic composition of several isolates further demonstrates that demarcation of the range boundary for the two main haplotype groups within C. briggsae does not strictly adhere to the Tropic of Cancer (Figure 5A) [19, 20]. Specifically, Chinese isolates GXW0023 and VX0033 from Wuhan (30°N) and GXW0024 from Weifang (36°N) clearly fall into the “Tropical/I” haplotype group, but are found farther north than most such isolates, and farther north even than some isolates from the “Temperate/II” haplotype group. Despite these exceptions, 93.6% of 141 “Tropical/I” isolates were collected in tropical or subtropical latitudes, and 100% of 72 “Temperate/II” isolates were collected in temperate latitudes. Interestingly, in addition to the more common “Tropical/I” isolates, the sets from Kerala, Hubei and Taiwan each included strains corresponding to distinct haplotype groups, suggesting that sampling at local scales might reveal substantial genetic diversity [16, 19]. This observed diversity motivated us to investigate local patterns of diversity of the C. briggsae isolates from French Guiana.
All C. briggsae isolated from French Guiana are nested within the "Tropical/I" phylogeographic group. The multi-locus analysis showed that they cluster into two sub-groups that mirror the pattern of differentiation observed circum-globally for “Tropical/I” isolates (“AF16-like” and “VT847-like;” Figure 5). The C. briggsae isolates from French Guiana thus harbour a great part of the genetic diversity found within "Tropical/I," despite the relatively small region sampled.
Within French Guiana, these two genetic sub-groups do not partition according to locality of origin. Indeed, diverse genotypes occurred at the two sites where several C. briggsae isolates were collected (i.e. both Nouragues and Montagne des Singes). In addition, we found little differentiation (F ST = 0.267) and divergence (D xy = 0.0020) between isolates from Nouragues and Montagne des Singes. Moreover, genotypes from the two genetic subgroups co-occurred at the smallest scale in the sub-sampling of Cecropia fruits (H6; italics in Figure 5B). Distinct genotypes also occurred at the scale of 5–10 metres in Montagne des Singes (NIC63 vs. NIC64). This result indicates that population structure among the French Guiana genotypes is not consistent with strong local population genetic differentiation that would lead to isolation by distance. Instead, the pattern of population genetic diversity of C. briggsae within French Guiana is consistent with it being a microcosm of pan-tropical diversity patterns, at least for the level of resolution permitted with single nucleotide polymorphism in nuclear loci. However, one multilocus genotype was dominant in the samples from Nouragues, which likely contributes to its non-zero differentiation with samples from Montagne des Singes (Figure 5B).
Population genetic summary statistics for different sample sets of C. briggsae , averaged across six nuclear loci
All French Guiana
High Caenorhabditisspecies richness in a tropical rainforest
Here we documented the extensive sampling of Caenorhabditis in a tropical rainforest in French Guiana and characterized the structure of genetic diversity of the cosmopolitan species C. briggsae from small (~1 m), intermediate (~1 km) and up to global spatial scales. We identified six species from a single tropical site, representing nearly 25% of the 26 Caenorhabditis species known in laboratory culture . Three of these species may be endemic to this region, although sampling of Caenorhabditis in South America is very limited. These findings reinforce the view that Caenorhabditis nematodes can be locally diverse and – although they have been generally referred to as soil nematodes – are more easily found in rotting vegetal matter, especially fruits, flowers and stems [3, 13].
Our sampling can be contrasted with a recent extensive sampling effort in temperate France . In mainland France, just two species of Caenorhabditis are found commonly: C. elegans and C. briggsae. In addition, C. remanei and C. sp. 13 each have been isolated once in the course of sampling many locations in France over many years . The isolation of six distinct Caenorhabditis species in just a few square kilometres of tropical forest, including three potentially endemic species, testifies to much higher species richness of Caenorhabditis in the tropics . Moreover, this finding for Caenorhabditis is fully consistent with latitudinal diversity patterns documented for many other taxa [25, 26]. As discovery of new species in this group is progressing rapidly, phylogenetically-informed analysis of Caenorhabditis species distributions may shed light on long-standing questions about the causes of latitudinal species diversity gradients .
Previous sporadic sampling of Caenorhabditis nematodes in Tropical South and Central America has yielded C. sp. 11, C. brenneri, and C. briggsae. An additional three species have also been found on Caribbean islands (C. sp. 14, C. sp. 19, and C. sp. 20) . The absence of the well-known C. elegans in the Nouragues Natural Reserve is not surprising, however, given that this species is rare in previous sampling from the tropics . Thus, the distribution of Caenorhabditis species around the world is consistent with there being a few cosmopolitan species and many other species endemic to particular geographic regions.
Our study demonstrates the first evidence of heterogeneous species distributions of Caenorhabditis at an intermediate spatial scale on the order of kilometres. It will be important in future work to determine whether these species distributions reflect stable features that might correspond to distinct ecological habitat characteristics of the different species, or instead reflect stochastic local abundances that are dynamic in time, perhaps owing to strong metapopulation dynamics associated with ephemeral food patches that can be utilized by many Caenorhabditis species. Co-occurrence of multiple species was common for samples of the same substrate type, and sometimes within the same sample, a pattern also reported for the less species-rich sampling in mainland France . These observations raise the neglected issue of niche space in Caenorhabditis biology as a major question to be answered to understand the abundance and distribution of species. Unfortunately, there are few data describing Caenorhabditis fitness reaction norms in relation to potential ecological factors that could differentially limit species persistence (e.g. temperature, bacterial food specificity, substrate chemistry) [13, 22, 28–30].
Spatial structure of genetic diversity
We used the cosmopolitan C. briggsae as a focal taxon for quantifying population genetic variability from the finest sampling scales within the Nouragues forest samples up to pooled samples at regional and global scales. We found that distinct C. briggsae genotypes co-exist at scales down to a few metres (Montagne des Singes) or even a single fruit (Nouragues, sample H6). Given their highly selfing mode of reproduction in nature [6, 13], this suggests that a given fruit can be colonized by multiple individuals of distinct genetic backgrounds. These results mirror findings for temperate latitude samples of C. elegans, in that high local diversity may occur while genetic differentiation among locations is low [8, 10, 11, 14, 31, 32]. This pattern of large-scale homogeneity coupled with fine-scale heterogeneity also is reminiscent of the 'chaotic genetic patchiness' observed for some intertidal invertebrates with a highly dispersing planktonic stage . In contrast to C. elegans, however, strong population structure dominates the global scale in C. briggsae, with 1) a large "Tropical/I" phylogeographic group distributed widely in the tropics around the world, 2) a large "Temperate/II" phylogeographic group having very low polymorphism overall and hence undetectable local diversity, and 3) a few genetically divergent clades, so far each found only in one place (Nairobi, Kenya; Montreal, Canada; Tai-an, Taiwan; Hubei, China; Kerala, India) [16, 19]. It is likely that such geographically restricted diversity is not yet exhausted by our sampling, nor are the possibilities for observing recombination among the main phylogeographic groups. Recombination had been previously noted at this large scale [6, 20] and can also be inferred among the French Guiana multilocus genotypes, as visualized by the reticulation pattern of the haplotype network (Figure 5B).
In this study, we described the first sampling of Caenorhabditis in a primary tropical forest environment, analysing a variety of substrates. We found six Caenorhabditis species, mostly in rotting flowers and fruits, the densest richness of species known in this group. Three of these species are cosmopolitan, three appear less widespread and might be endemic to French Guiana. The genetic structure of C. briggsae populations indicates events of long-distance migrations among different continents in the tropical zone, and a local spatial structure resembling that described for C. elegans in temperate zone populations.
Sampling sites in French Guiana
Samples were collected between November 17 and 27, 2009 at the end of the dry season. Most samples were collected at the CNRS “Inselberg” field station in the Nouragues Natural Reserve (4.08809°N, -52.6796°W) within an area of approximately four square kilometres (Figure 3). We also collected samples at other locations, including mangrove forests in the outskirts of Cayenne (Montabo trail), secondary forests (e.g. Montagne des Singes, Kourou), and agricultural areas around the village of Cacao (Figure 1).
Sample collection and analysis
We collected a variety of rotting plant material, primarily targeting rotting fruits and flowers. Such substrates are known to frequently harbour Caenorhabditis (Additional files 1 and 2). Samples were collected, photographed and stored in plastic zip bags. A given sample identifier code refers to a substrate sample (e.g. a single or multiple fruits) at a single location of a few square metres, contained within a single bag. Part of the samples were analysed at the Nouragues field station using a dissecting microscope and ready-to-use 35 mm C. elegans Normal Growth Medium (NGM) culture plates previously seeded with E. coli OP50 , allowing us to determine developmental stages and number of individuals present at the time of isolation. The other samples were stored for the duration of the field trip (14 days) and examined afterwards in the laboratories in Nice and Paris, using 55 and 90 mm culture plates. Samples were spread around the lawn and 1–2 ml of water or M9 solution was added to the samples. All plates were examined regularly using the dissecting microscope, and nematodes were isolated over a period of seven days. Note that all C. briggsae isolates used for genetic analysis (see below) were derived from independent substrate samples, except for one sample (G2) from which eight C. briggsae isolates were derived from different individuals, immediately after isolation on site (isolates NIC23, NIC28, NIC29, NIC30, NIC36, NIC37, NIC38, NIC40) (Additional file 2). This sampling protocol ensured that any potential genetic differences found among isolates indicate the presence of genetically distinct natural isolates in the same substrate sample.
Species identification and isolate establishment
Caenorhabditis genus identity was confirmed by microscopy using morphological criteria . Species identity was further examined through mating tests with known species and/or ITS2 sequencing as described previously . (Note that newly discovered species are attributed a number before a formal taxonomic description has been published). Stock cultures were established by isolation of a single hermaphrodite or female. For gonochoristic species, we picked either a female with a copulatory plug, or one female and one male. The mode of reproduction was determined by isolating virgin L4 females/hermaphrodites and scoring for the absence/presence of progeny. For androdioecious species, isogenic strains (referred to as “isolate”) were produced by isolating a single larva for a few (3–6) generations. For gonochoristic species, strains were established as isofemale lines. From each isolated Caenorhabditis sample, we established cultures, which were cryopreserved and stocked in our collections.
A complete list of isolates can be found in Additional file 2. JU isolates are stored in the lab of MAF and NIC isolates are stored in the lab of CB. All worm strains are available upon request.
Geographically localised (“small-scale”) sampling of Cecropiafruits in the Nouragues forest
To examine the species distribution and genetic diversity of C. briggsae at different spatial scales, we collected a large number of samples from rotting fruits of Cecropia sp. (likely Cecropia sciadophylla) at two sites in the Nouragues Natural Reserve from which we had previously collected C. briggsae and other Caenorhabditis species (Sample ID H3, H6; Additional file 2). The forest ground at these two sites was covered by numerous rotting Cecropia fruits of black or sometimes brown colour. At each site, we collected 11 individual rotting fruits from the ground within an area of approximately 40 m2 (fruits were separated from each other by approx. 2–8 m). From six of these fruits, we derived sub-samples by collecting separately five small fruit parts ("fingers") from each fruit. From both sampling sites, we also collected three litter samples (consisting primarily of rotting leaves) and three humus samples. For one of the sites (samples H3), we further collected four invertebrate samples: one live snail, two snail shells, and one live myriapod. Collection of independent subsamples of each substrate sample on site allowed subsequent analysis to detect potential mixing of different genotypes in the same sample. For details of sampling design, see Figure 4.
Additional C. briggsaeisolates analysed
We further included 46 new C. briggsae isolates, mostly collected from rotting vegetation, from localities across five continents; including eight regions not previously sampled for Caenorhabditis nematodes (Additional file 3). Each isolate was founded from a single hermaphrodite individual, maintained using standard protocols, and taxonomic status was determined by mating tests and/or ITS2 sequencing . The geographic and ecological information of the wild isolates was also entered in Wormbase (http://www.wormbase.org). An interactive map of collection localities and isolate information can be found online (C. briggsae: https://www.google.com/maps/ms?msa=0&msid=117700919974655793194.00046c7ccc0afccc319b7&t=h&z=2).
DNA amplification and sequencing
Gene fragments corresponding to the six loci used in previous studies of C. briggsae diversity were amplified and sequenced using published primers . DNA was isolated from large populations of isogenic worms of each strain using the DNeasy Blood and Tissue kit (Qiagen). Amplifications were processed in 30 μL reaction volumes with 1.5 μL DMSO, 3 μL dNTPs (6.6 mM), 3 μL 10X Buffer (Fermentas), 2.4 μL MgCl2, 0.36 μL of each primer (50 μM), 0.18 μL of Taq polymerase (New England Biolabs) and 2 μL of genomic DNA. Cycling conditions were: 95°C for 4 min followed by 35 cycles of 95°C for 1 min, 55°C or 58°C for 1 min and 72°C for 1 min. Amplifications were sequenced at the University of Arizona UAGC sequencing facility. All markers were sequenced on both strands and all polymorphisms were visually verified using sequencing chromatograms. Primer sequences were manually deleted from each sequence prior to analysis. All new sequences are accessible in GenBank with accession numbers JX288123-JX288761.
We analysed a total of 99 new wild isolates of C. briggsae (53 from French Guiana, 46 from other world-wide localities). Note that four French Guiana isolates (NIC88, NIC106, NIC107, NIC108) were analysed in Jovelin & Cutter . Based on a set of six nuclear loci used previously [6, 16, 17, 19], we investigated the relationships of the 57 new isolates for which data were collected for all six loci, relative to a collection of 132 isolates that were used in previous studies on C. briggsae diversity [6, 16, 17, 19]. We also obtained sequence data for up to five of these loci for the remaining new isolates, which informed some analyses (Additional file 3). Multiple sequence alignments were constructed for each locus in BioEdit  and manually edited for indel polymorphisms. We inferred the relationships among isolates with concatenated sequences from the set of six loci using unrooted neighbour-networks generated with a Jukes-Cantor distance in the program SplitsTree 4.10 . Neighbour-networks are useful for representing the relationships among individuals of the same species for which recombination events may be non-negligible . We then measured differentiation and divergence between phylogeographic groups using F ST  and D xy , the average number of nucleotide substitutions per site between groups . We also measured nucleotide polymorphism  at each locus taken separately using DnaSP v.5  and took the average across loci in order to investigate nucleotide diversity at multiple spatial scales in C. briggsae.
MAF and CB acknowledge financial support by the CNRS, including a grant for research at the Nouragues field station, and would like to thank the staff at the station and the CNRS in French Guiana, in particular, Patrick Châtelet, Philippe Gaucher and Jérôme Chave. We also thank those who provided access to sampling sites (Bruno Le Vessier) and information on sampled fruits (Pierre-Michel Forget). We are grateful to Matt Rockman for the New Jersey isolates and to Patrick Châtelet, Mathieu Joron, Didier Peigne, Christopher Nelson, Amir Yassin for collecting samples. CB is funded by the CNRS, Agence Nationale de la Recherche and the Fondation Schlumberger pour l'Education et la Recherche. ADC received support from the Natural Sciences and Engineering Research Council (NSERC) of Canada and from a Canada Research Chair. RJ was supported by an Ontario Ministry of Research and Innovation postdoctoral fellowship and SH was supported by a University of Toronto Excellence Award. ECA was supported by a Ruth L. Kirschstein National Research Service Award post-doctoral fellowship (F32-GM089007) and training grant T32-CA009528 from the National Cancer Institute.
- Cutter AD, Dey A, Murray RL: Evolution of the Caenorhabditis elegans genome. Mol Biol Evol. 2009, 26 (6): 1199-1234. 10.1093/molbev/msp048.PubMedView Article
- Félix M-A, Braendle C: The natural history of Caenorhabditis elegans. Curr Biol. 2010, 20: R965-R969. 10.1016/j.cub.2010.09.050.PubMedView Article
- Kiontke K, Félix M-A, Ailion M, Rockman MV, Braendle C, Pénigault J-B, Fitch DH: A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evol Biol. 2011, 11: 339-10.1186/1471-2148-11-339.PubMed CentralPubMedView Article
- Kiontke K, Sudhaus W: Ecology of Caenorhabditis species. Wormbook. 2006, The C. elegans Research Community, http://www.wormbook.org,
- Barrière A, Félix M-A: Natural variation and population genetics of C. elegans. Wormbook. 2005, The C. elegans Research Community, http://www.wormbook.org,
- Cutter AD: Nucleotide polymorphism and linkage disequilibrium in wild populations of the partial selfer Caenorhabditis elegans. Genetics. 2006, 172 (1): 171-184.PubMed CentralPubMedView Article
- Graustein A, Gaspar JM, Walters JR, Palopoli MF: Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics. 2002, 161 (1): 99-107.PubMed CentralPubMed
- Haber M, Schüngel M, Putz A, Müller S, Hasert B, Schulenburg H: Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding. Mol Biol Evol. 2005, 22: 160-173.PubMedView Article
- Jovelin R, Ajie BC, Phillips PC: Molecular evolution and quantitative variation for chemosensory behaviour in the nematode genus Caenorhabditis. Mol Ecol. 2003, 12 (5): 1325-1337. 10.1046/j.1365-294X.2003.01805.x.PubMedView Article
- Sivasundar A, Hey J: Sampling from natural populations with RNAI reveals high outcrossing and population structure in Caenorhabditis elegans. Curr Biol. 2005, 15 (17): 1598-1602. 10.1016/j.cub.2005.08.034.PubMedView Article
- Barrière A, Felix M-A: Temporal dynamics and linkage disequilibrium in natural C. elegans populations. Genetics. 2007, 176: 999-1011.PubMed CentralPubMedView Article
- Caswell-Chen EP, Chen J, Lewis EE, Douhan GW, Nadler SA, Carey JR: Revising the standard wisdom of C. elegans natural history: ecology of longevity. Sci Aging Knowl Environ. 2005, 40: pe30-
- Félix MA, Duveau F: Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. BMC Biol. 2012, 10 (1): 59-10.1186/1741-7007-10-59.PubMed CentralPubMedView Article
- Andersen EC, Gerke JP, Shapiro JA, Crissman JR, Ghosh R, Bloom JS, Felix MA, Kruglyak L: Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nat Genet. 2012, 44: 285-290. 10.1038/ng.1050.PubMed CentralPubMedView Article
- Phillips PC: Self-fertilization sweeps up variation in the worm genome. Nat Genet. 2012, 44 (3): 237-238. 10.1038/ng.2201.PubMed CentralPubMedView Article
- Cutter AD, Yan W, Tsvetkov N, Sunil S, Felix MA: Molecular population genetics and phenotypic sensitivity to ethanol for a globally diverse sample of the nematode Caenorhabditis briggsae. Mol Ecol. 2010, 19 (4): 798-809. 10.1111/j.1365-294X.2009.04491.x.PubMedView Article
- Dolgin ES, Felix MA, Cutter AD: Cutter Hakuna Nematoda: genetic and phenotypic diversity in African isolates of Caenorhabditis elegans and C. briggsae. Heredity. 2008, 100 (3): 304-315. 10.1038/sj.hdy.6801079.PubMedView Article
- Howe DK, Denver DR: Muller's Ratchet and compensatory mutation in Caenorhabditis briggsae mitochondrial genome evolution. BMC Evol Biol. 2008, 8: 62-10.1186/1471-2148-8-62.PubMed CentralPubMedView Article
- Jovelin R, Cutter AD: MicroRNA sequence variation potentially contributes to within-species functional divergence in the nematode Caenorhabditis briggsae. Genetics. 2011, 189 (3): 967-976. 10.1534/genetics.111.132795.PubMed CentralPubMedView Article
- Raboin MJ, Timko AF, Howe DK, Felix MA, Denver DR: Evolution of Caenorhabditis mitochondrial genome pseudogenes and Caenorhabditis briggsae natural isolates. Mol Biol Evol. 2010, 27 (5): 1087-1096. 10.1093/molbev/msp318.PubMed CentralPubMedView Article
- Dey A, Jeon Y, Wang GX, Cutter AD: Global population genetic structure of Caenorhabditis remanei reveals incipient speciation. Genetics. 2012, 191 (4): 1257-1269. 10.1534/genetics.112.140418.PubMed CentralPubMedView Article
- Prasad A, Croydon-Sugarman MJ, Murray RL, Cutter AD: Temperature-dependent fecundity associates with latitude in Caenorhabditis briggsae. Evolution. 2011, 65 (1): 52-63. 10.1111/j.1558-5646.2010.01110.x.PubMedView Article
- Stadler T, Haubold B, Merino C, Stephan W, Pfaffelhuber P: The impact of sampling schemes on the site frequency spectrum in nonequilibrium subdivided populations. Genetics. 2009, 182 (1): 205-216. 10.1534/genetics.108.094904.PubMed CentralPubMedView Article
- Cutter AD, Wang GX, Ai H, Peng Y: Influence of finite-sites mutation, population subdivision and sampling schemes on patterns of nucleotide polymorphism for species with molecular hyperdiversity. Mol Ecol. 2012, 21 (6): 1345-1359. 10.1111/j.1365-294X.2012.05475.x.PubMedView Article
- Gaston KJ: Global patterns in biodiversity. Nature. 2000, 405 (6783): 220-227. 10.1038/35012228.PubMedView Article
- Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM, Bush MB, Harrison SP, Hurlbert AH, Knowlton N, Lessios HA, et al: Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol Lett. 2007, 10 (4): 315-331. 10.1111/j.1461-0248.2007.01020.x.PubMedView Article
- Weir JT, Schluter D: The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science. 2007, 315 (5818): 1574-1576. 10.1126/science.1135590.PubMedView Article
- Anderson JL, Albergotti L, Ellebracht B, Huey RB, Phillips PC: Does thermoregulatory behavior maximize reproductive fitness of natural isolates of Caenorhabditis elegans?. BMC Evol Biol. 2011, 11: 157-10.1186/1471-2148-11-157.PubMed CentralPubMedView Article
- Fodor A, Riddle DL, Nelson FK, Golden JW: Comparison of a new wild-type Caenorhabditis briggsae with laboratory strains of Caenorhabditis briggsae and Caenorhabditis elegans. Nematologica. 1983, 29: 203-217. 10.1163/187529283X00456.View Article
- Grewal PS: Influence of bacteria and temperature on the reproduction of Caenorhabditis elegans (Nematoda: Rhabditidae) infesting mushrooms (Agaricus bisporus). Nematologica. 1991, 37: 72-82. 10.1163/187529291X00079.View Article
- Barrière A, Félix M-A: High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr Biol. 2005, 15: 1176-1184. 10.1016/j.cub.2005.06.022.PubMedView Article
- Cutter AD, Félix M-A, Barrière A, Charlesworth D: Patterns of nucleotide polymorphism distinguish temperate and tropical wild isolates of Caenorhabditis briggsae. Genetics. 2006, 173: 2021-2031. 10.1534/genetics.106.058651.PubMed CentralPubMedView Article
- Johnson MS, Black R: Chaotic genetic patchiness in an intertidal limpet, Siphonaria sp. Mar Biol. 1982, 70: 157-164. 10.1007/BF00397680.View Article
- Barrière A, Félix M-A: Isolation of C. elegans and related nematodes. Wormbook. 2006, The C. elegans Research Community, http://www.wormbook.org]
- Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999, 41: 95-98.
- Huson DH, Bryant D: Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006, 23 (2): 254-267.PubMedView Article
- Huson DH, Scornavacca C: A survey of combinatorial methods for phylogenetic networks. Genome Biol Evol. 2011, 3: 23-35. 10.1093/gbe/evq077.PubMed CentralPubMedView Article
- Wright S: The genetical structure of populations. Ann Eugenics. 1951, 15: 323-354.View Article
- Nei M: Molecular Evolutionary Genetics. 1987, New York: Columbia University Press
- Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009, 25 (11): 1451-1452. 10.1093/bioinformatics/btp187.PubMedView Article
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.