Whole-genome sequencing reveals the extent of heterozygosity in a preferentially self-fertilizing hermaphroditic vertebrate
Open accessAbstract
The mangrove rivulus, Kryptolebias marmoratus, is one of only two self-fertilizing hermaphroditic fish species and inhabits mangrove forests. While selfing can be advantageous, it reduces heterozygosity and decreases genetic diversity. Studies using microsatellites found that there are variable levels of selfing among populations of K. marmoratus, but overall, there is a low rate of outcrossing and, therefore, low heterozygosity. In this study, we used whole-genome data to assess the levels of heterozygosity in different lineages of the mangrove rivulus and infer the phylogenetic relationships among those lineages. We sequenced whole genomes from 15 lineages that were completely homozygous at microsatellite loci and used single nucleotide polymorphisms (SNPs) to determine heterozygosity levels. More variation was uncovered than in studies using microsatellite data because of the resolution of full genome sequencing data. Moreover, missense polymorphisms were found most often in genes associated with immune function and reproduction. Inferred phylogenetic relationships suggest that lineages largely group by their geographic distribution. The use of whole-genome data provided further insight into genetic diversity in this unique species. Although this study was limited by the number of lineages that were available, these data suggest that there is previously undescribed variation within lineages of K. marmoratus that could have functional consequences and (or) inform us about the limits to selfing (e.g., genetic load, accumulation of deleterious mutations) and selection that might favor the maintenance of heterozygosity. These results highlight the need to sequence additional individuals within and among lineages.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
HON fish and those from the FW site in Belize are genetically distinct.
“HON fish and those from the FW site in Belize are genetically distinct (Lins et al., 2018).”
From Genomic and physiological mechanisms underlying skin plasticity during water to air transition in an amphibious fish (2020) · cites this paper as Lins et al., 2018
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
The Sequence Alignment/Map format and SAMtools
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., Durbin, R., & 1000 Genome Project Data Processing Subgroup (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp352 · Cited by 62,041 · see citing works
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Edgar, R. C. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh340 · Cited by 44,662 · see citing works
PLINK: a tool set for whole-genome association and population-based linkage analyses.
Purcell, S., Neale, B., Todd-Brown, K., Thomas, L., Ferreira, M. A. R., Bender, D., Maller, J., Sklar, P., de Bakker, P. I. W., Daly, M. J., et al. (2007) · The American Journal of Human Genetics · doi:10.1086/519795 · Cited by 34,089 · see citing works
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
Stamatakis, A. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu033 · Cited by 32,291 · see citing works
MrBayes 3: Bayesian phylogenetic inference under mixed models
Ronquist, F., & Huelsenbeck, J. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg180 · Cited by 28,956 · see citing works
The variant call format and VCFtools
Danecek, P., Auton, A., Abecasis, G. R., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G. A., Marth, G., Sherry, S. T., et al. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr330 · Cited by 16,008 · see citing works
Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J., & Pachter, L. (2010) · Nature Biotechnology · doi:10.1038/nbt.1621 · Cited by 15,556 · see citing works
Second-generation PLINK: rising to the challenge of larger and richer datasets
Chang, C. C., Chow, C. C., Tellier, L. C., Vattikuti, S., Purcell, S. M., & Lee, J. J. (2015) · Gigascience · doi:10.1186/s13742-015-0047-8 · Cited by 12,709 · see citing works
Cingolani, P., Platts, A., Wang, L. L., Coon, M., Nguyen, T., Wang, L., Land, S. J., Lu, X., & Ruden, D. M. (2012) · Fly · doi:10.4161/fly.19695 · Cited by 11,816 · see citing works
Aligning sequence reads, clone sequences and assembly contigs with BWA-MEMPreprint
Li, H. (2013) · arXiv (Cornell University) · doi:10.48550/arxiv.1303.3997 · Cited by 9,540 · see citing works
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., & Calcott, B. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msw260 · Cited by 5,242 · see citing works
UniProt: the universal protein knowledgebase
The UniProt Consortium (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw1099 · Cited by 4,436 · see citing works
High-throughput functional annotation and data mining with the Blast2GO suite
Götz, S., Garcia-Gomez, J. M., Terol, J., Williams, T., Nagaraj, S. H., Nueda, M. J., Robles, M., Talón, M., Dopazo, J., & Conesa, A. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn176 · Cited by 4,395 · see citing works
Robust relationship inference in genome-wide association studies
Manichaikul, A., Mychaleckyj, J. C., Rich, S. S., Daly, K., Sale, M., & Chen, W.-M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq559 · Cited by 3,541 · see citing works
Inference of population splits and mixtures from genome-wide allele frequency data
Pickrell, J. K., & Pritchard, J. K. (2012) · PLoS Genetics · doi:10.1371/journal.pgen.1002967 · Cited by 2,731 · see citing works
Iwasaki, W., Fukunaga, T., Isagozawa, R., Yamada, K., Maeda, Y., Satoh, T., Sado, T., Mabuchi, K., Takeshima, H., Miya, M. U., et al. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst141 · Cited by 866 · see citing works
FASconCAT: Convenient handling of data matrices
Kück, P., & Meusemann, K. (2010) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2010.04.024 · Cited by 539 · see citing works
Jun, G., Flickinger, M., Hetrick, K. N., Romm, J. M., Doheny, K. F., Abecasis, G. R., Boehnke, M., & Kang, H. M. (2012) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2012.09.004 · Cited by 484 · see citing works
Inbreeding and runs of homozygosity: A possible solution to an old problem
Čurik, I., Ferenčaković, M., & Sölkner, J. (2014) · Livestock Science · doi:10.1016/j.livsci.2014.05.034 · Cited by 419 · see citing works
Long Runs of Homozygosity Are Enriched for Deleterious Variation
Szpiech, Z. A., Xu, J., Pemberton, T. J., Peng, W., Zöllner, S. K., Rosenberg, N. A., & Li, J. Z. (2013) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2013.05.003 · Cited by 335 · see citing works
Oviparous Hermaphroditic Fish with Internal Self-Fertilization
Harrington, R. W. (1961) · Science · doi:10.1126/science.134.3492.1749 · Cited by 201 · see citing works
The mating system and microevolution.
Rw, A. (1975) · PubMed · Cited by 186 · see citing works
Evolution of Selfing: Recurrent Patterns in Molecular Adaptation
Shimizu, K. K., & Tsuchimatsu, T. (2015) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-112414-054249 · Cited by 146 · see citing works
Genetic variation in clonal vertebrates detected by simple-sequence DNA fingerprinting.
Turner, B. J., Elder, J. F., Laughlin, T. F., & Davis, W. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.15.5653 · Cited by 127 · see citing works
Mackiewicz, M., Tatarenkov, A., Taylor, D. S., Turner, B. J., & Avise, J. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603847103 · Cited by 126 · see citing works
Self-citationHarrington, R. W. (1967) · Biological Bulletin · doi:10.2307/1539887 · Cited by 126 · see citing works
Taylor, D. S. (2012) · Integrative and Comparative Biology · doi:10.1093/icb/ics062 · Cited by 121 · see citing works
Emersion in the mangrove forest fishRivulus marmoratus: a unique response to hydrogen sulfide
Abel, D. C., Koenig, C. C., & Davis, W. P. (1987) · Environmental Biology of Fishes · doi:10.1007/bf00002329 · Cited by 97 · see citing works
Lee, J., Miya, M. U., Lee, Y.-S., et al. (2001) · Gene · doi:10.1016/s0378-1119(01)00765-x · Cited by 96 · see citing works
Tatarenkov, A., Ring, B. C., Elder, J. F., Bechler, D. L., & Avise, J. C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012863 · Cited by 89 · see citing works
Self-citationA mixed-mating strategy in a hermaphroditic vertebrate
Mackiewicz, M., Tatarenkov, A., Turner, B. J., & Avise, J. C. (2006) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2006.3594 · Cited by 78 · see citing works
Self-citationBEST OF BOTH WORLDS? ASSOCIATION BETWEEN OUTCROSSING AND PARASITE LOADS IN A SELFING FISH
Ellison, A., Cable, J., & Consuegra, S. (2011) · Evolution · doi:10.1111/j.1558-5646.2011.01354.x · Cited by 65 · see citing works
Outcrossing in a Natural Population of a Self-Fertilizing Hermaphroditic Fish
Lubinski, B. A., Davis, W. P., Taylor, D. S., et al. (1995) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a111623 · Cited by 60 · see citing works
Harrington, R. W. (1968) · Physiological Zoology · doi:10.1086/physzool.41.4.30155480 · Cited by 57 · see citing works
Molecular Evolution of Freshwater Snails with Contrasting Mating Systems
Burgarella, C., Gayral, P., Ballenghien, M., Bernard, A., David, P., Jarne, P., Correa, A. C., Hurtrez‐Boussès, S., Escobar, J. S., Galtier, N., et al. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv121 · Cited by 56 · see citing works
Kelley, J. L., Yee, M., Brown, A. P. C., Richardson, R., Tatarenkov, A., Lee, C. C., Harkins, T. T., Bustamante, C. D., & Earley, R. L. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw145 · Cited by 56 · see citing works
Self-citationTatarenkov, A., GAO, H., Mackiewicz, M., Taylor, D. S., Turner, B. J., & Avise, J. C. (2007) · Molecular Ecology · doi:10.1111/j.1365-294x.2007.03349.x · Cited by 54 · see citing works
Self-citationNoël, E., Jarne, P., Glémin, S., MacKenzie, A., Ségard, A., Sarda, V., & David, P. (2016) · Current Biology · doi:10.1016/j.cub.2016.11.015 · Cited by 54 · see citing works
Vrijenhoek, R. C. (1985) · Journal of Heredity · doi:10.1093/oxfordjournals.jhered.a110050 · Cited by 53 · see citing works
Tatarenkov, A., Earley, R. L., Taylor, D. S., et al. (2012) · Integrative and Comparative Biology · doi:10.1093/icb/ics075 · Cited by 49 · see citing works
Self-citationEpigenetic regulation of sex ratios may explain natural variation in self-fertilization rates
Ellison, A., Lopez, C. M. R., Morán, P., et al. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.1900 · Cited by 46 · see citing works
Ellison, A., Allainguillaume, J., GIRDWOOD, S. E., Pachebat, J. A., Peat, K. M., Wright, P. A., & Consuegra, S. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.1929 · Cited by 45 · see citing works
Turner, B. J., Fisher, M. T., Taylor, D. S., et al. (2006) · Evolutionary ecology research · Cited by 44 · see citing works
Hunter, S. S., Lyon, R. T., Sarver, B. A. J., et al. (2015) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/014662 · Cited by 43 · see citing works
Tatarenkov, A., Earley, R. L., Perlman, B. M., et al. (2015) · Journal of Heredity · doi:10.1093/jhered/esv013 · Cited by 35 · see citing works
Self-citationTatarenkov, A., Lima, S. M. Q., Earley, R. L., Berbel‐Filho, W. M., Vermeulen, F. B. M., Taylor, D. S., Marson, K. M., Turner, B. J., & Avise, J. C. (2017) · Biological Journal of the Linnean Society · doi:10.1093/biolinnean/blx103 · Cited by 30 · see citing works
Self-citationChoosy Males Could Help Explain Androdioecy in a Selfing Fish
Ellison, A., Jones, J., Inchley, C. E., et al. (2013) · The American Naturalist · doi:10.1086/670304 · Cited by 29 · see citing works
Rhee, J., Choi, B., Kim, J., Kim, B., Lee, Y., Kim, I., Kanamori, A., Choi, I., Schartl, M., & Lee, J. (2017) · Scientific Reports · doi:10.1038/srep40121 · Cited by 29 · see citing works
A Genetic Test for Whether Pairs of Hermaphrodites Can Cross-Fertilize in a Selfing Killifish
Furness, A. I., Tatarenkov, A., & Avise, J. C. (2015) · Journal of Heredity · doi:10.1093/jhered/esv077 · Cited by 28 · see citing works
Self-citationSato, A., Satta, Y., Figueroa, F., et al. (2002) · Genetics · doi:10.1093/genetics/162.4.1791 · Cited by 23 · see citing works
Avise, J. C., & Tatarenkov, A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217202109 · Cited by 22 · see citing works
Self-citationMale-Male Competition in a Mixed-Mating Fish
Molloy, P. P., Nyboer, E. A., & Côté, I. M. (2011) · Ethology · doi:10.1111/j.1439-0310.2011.01916.x · Cited by 17 · see citing works
Factors affecting egg production in the selfing mangrove rivulus (Kryptolebias marmoratus)
Lomax, J. L., Carlson, R. E., Wells, J. W., et al. (2017) · Zoology · doi:10.1016/j.zool.2017.02.004 · Cited by 15 · see citing works
Tatarenkov, A., Mesak, F., & Avise, J. C. (2015) · Mitochondrial DNA Part A · doi:10.3109/19401736.2015.1115861 · Cited by 7 · see citing works
Self-citationKim, H.-S., Hwang, D., Hagiwara, A., et al. (2016) · Mitochondrial DNA Part B · doi:10.1080/23802359.2016.1197075 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dong, Y.-W., Blanchard, T. S., Noll, A., Vasquez, P., Schmitz, J., Kelly, S. P., Wright, P. A., & Whitehead, A. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.235515 · Cited by 18 · see citing works
- Authors
- Lins, L. S. F., Trojahn, S., Sockell, A., Yee, M.-C., Tatarenkov, A., Bustamante, C. D., Earley, R. L., & Kelley, J. L.
- Affiliations
- Washington State University (US)
- Stanford University (US)
- University of California, Irvine (US)
- University of Alabama (US)
- Corresponding author
- Lins, Luana S.F.
- Trojahn, Shawn
- ORCID
- Venue
- Genome
- Publisher
- Canadian Science Publishing
- Published
- 2018-04
- Volume
- 61
- Issue
- 4
- Pages
- 241-247
- ISSN
- 0831-2796 (ISSN-L)
- 1480-3321
- OpenAlex
- W2777707236
- Cited by
- 18
- References
- 56
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 5 · 2019: 3 · 2018: 3
- FWCI
- 1.99
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genome (publishedVersion)
- PubMed (publishedVersion)
- TSpace (University of Toronto) (acceptedVersion)
- TSpace (University of Toronto) (submittedVersion)
- Funders
- National Science Foundation (1347973)
- University of Alabama
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- Kryptolebias marmoratus, mangrove rivulus, self-fertilization, heterozygosity, hermaphroditic fish, genetic diversity, single nucleotide polymorphisms, missense polymorphisms, immune-related genes, reproductive genes, phylogenetic relationships, genetic load, deleterious mutations, outcrossing
- MeSH terms
- Whole Genome Sequencing, Animals, Cyprinodontiformes, Geography, Heterozygote, Homozygote, Phylogeny, Vertebrates, Genome, Caribbean Region, Microsatellite Repeats, Polymorphism, Single Nucleotide, Hermaphroditic Organisms, Self-Fertilization
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
