Natural variants of C. elegans demonstrate defects in both sperm function and oogenesis at elevated temperatures

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Petrella, Lisa N ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Marquette University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CAENORHABDITIS ELEGANS; CELL FUNCTION; CONTROLLED STUDY; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; GERM LINE; HEAT SENSITIVITY; HEAT TOLERANCE; HERMAPHRODITE; MALE; MALE FERTILITY; NONHUMAN; OOCYTE DEVELOPMENT; PARASITE ISOLATION; SPERMATOGENESIS; SPERMATOZOON; TEMPERATURE SENSITIVITY; ADAPTATION; ANIMAL; CLASSIFICATION; CLIMATE; FEMALE; FERTILITY; GENETICS; GEOGRAPHY; METABOLISM; PHYSIOLOGY; REPRODUCTION; TEMPERATURE;

CAENORHABDITIS ELEGANS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CAENORHABDITIS ELEGANS; CLIMATE; FEMALE; FERTILITY; GENOTYPE; GEOGRAPHY; HERMAPHRODITIC ORGANISMS; MALE; OOGENESIS; REPRODUCTION; SPERMATOZOA; TEMPERATURE;

EID: 84911363042     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112377     Document Type: Article

References (32)

1. Kim B, Park K, Rhee K (2012) Heat stress response of male germ cells. Cell Mol Life Sci 70: 2623-2636. doi: 10.1007/s00018-012-1165-4
2. David JR, Araripe LO, Chakir M, Legout H, Lemos B, et al. (2005) Male sterility at extreme temperatures: a significant but neglected phenomenon for understanding Drosophila climatic adaptations. J Evolution Biol 18: 838-846. doi: 10.1111/j.1420-9101.2005.00914.x
3. Harvey SC, Viney ME (2007) Thermal variation reveals natural variation between isolates of Caenorhabditis elegans. J Exp Zool B Mol Dev Evol 308: 409-416. doi: 10.1002/jez.b.21161
4. Prasad A, Croydon-Sugarman MJF, Murray RL, Cutter AD (2010) Temper-ature- dependent fecundity associates with latitude in Caenorhabditis briggsae. Evolution 65: 52-63. doi: 10.1111/j.1558-5646.2010.01110.x
5. Kiontke KC, Félix M-A, Ailion M, Rockman MV, Braendle C, et al. (2011) A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits. BMC Evolutionary Biology 11: 339. doi: 10.1186/ 1471-2148-11-339
6. Fe?lix M-A, Duveau F (2012) Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. BMC Biology 10: 59. doi: 10.1186/1741-7007-10-59
7. Gupta (2007) Genomics and biology of the nematode Caenorhabditis briggsae. WormBook. doi: 10.1895/wormbook.1.136.1
8. Chen J, Lewis EE, Carey JR, Caswell H, Caswell-Chen EP (2006) The ecology and biodemography of Caenorhabditis elegans. Experimental Gerontology 41: 1059-1065. doi: 10.1016/j.exger.2006.07.005
9. Rohmer C, David JR, Moreteau B, Joly D (2004) Heat induced male sterility in Drosophila melanogaster: adaptive genetic variations among geographic populations and role of the Y chromosome. J Exp Biol 207: 2735-2743. doi: 10.1242/jeb.01087
10. McMullen PD, Aprison EZ, Winter PB, Amaral LAN, Morimoto RI, et al. (2012) Macro-level Modeling of the Response of C. elegans Reproduction to Chronic Heat Stress. PLoS Comput Biol 8: e1002338. doi: 10.1371/journal. pcbi.1002338.s008
11. ARARIPE LO, Klaczko LB, MORETEAU B, David JR (2004) Male sterility thresholds in a tropical cosmopolitan drosophilid, Zaprionus indianus. Journal of Thermal Biology 29: 73-80. doi: 10.1016/j.jtherbio.2003.11.006
12. Dolgin ES, Fe?lix M-A, Cutter AD (2007) Hakuna Nematoda: genetic and phenotypic diversity in African isolates of Caenorhabditis elegans and C. briggsae. Heredity 100: 304-315. doi: 10.1038/sj.hdy.6801079
13. Anderson JL, Albergotti L, Proulx S, Peden C, Huey RB, et al. (2007) Thermal preference of Caenorhabditis elegans: a null model and empirical tests. Journal of Experimental Biology 210: 3107-3116. doi: 10.1242/jeb.007351
14. Andersen EC, Gerke JP, Shapiro JA, Crissman JR, Ghosh R, et al. (2012) Chromosome-scale selective sweeps shape Caenorhabditis elegans genomic diversity. Nature Genetics: 1-8. doi: 10.1038/ng.1050
15. Waddington CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150: 563-565.
16. Debat V, David P (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends in Ecology & Evolution 16: 555-561.
17. Dworkin I (2005) A study of canalization and developmental stability in the sternopleural bristle system of Drosophila melanogaster. Evolution 59: 1500-1509.
18. Ramler D, Mitteroecker P, Shama LNS, Wegner KM, Ahnelt H (2014) Nonlinear effects of temperature on body form and developmental canalization in the threespine stickleback. J Evolution Biol. doi: 10.1111/jeb.12311
19. Bronikowski A, Vleck D (2010) Metabolism, Body Size and Life Span: A Case Study in Evolutionarily Divergent Populations of the Garter Snake (Thamnophis elegans). Integrative and Comparative Biology 50: 880-887. doi: 10.1093/icb/ icq132
20. Gibson G, Wagner G (2000) Canalization in evolutionary genetics: a stabilizing theory? Bioessays 22: 372-380. doi: 10.1002/(SICI)1521-1878(200004)22: 4, 372::AID- BIES7.3.0.CO; 2-J.
21. Sollars V, Lu X, Xiao L, Wang X, Garfinkel MD, et al. (2002) Evidence for an epigenetic mechanism by which Hsp90 acts as a capacitor for morphological evolution. Nature Genetics 33: 70-74. doi: 10.1038/ng1067
22. Wong KS, Houry WA (2006) Hsp90 at the crossroads of genetics and epigenetics. Cell Res 16: 742-749. doi: 10.1038/sj.cr.7310090
23. Chakir M, Chafik A, Moreteau B, Gibert P, David JR (2002) Male sterility thermal thresholds in Drosophila: D. simulans appears more cold-adapted than its sibling D. melanogaster. Genetica 114: 195-205.
24. Chatterjee I, Ibanez-Ventoso C, Vijay P, Singaravelu G, Baldi C, et al. (2013) Dramatic fertility decline in aging C. elegans males is associated with mating execution deficits rather than diminished sperm quality. EXG 48: 1156-1166. doi: 10.1016/j.exger.2013.07.014
25. Yaeram J, Setchell BP, Maddocks S (2006) Effect of heat stress on the fertility of male mice in vivoand in vitro. Reprod Fertil Dev 18: 647. doi: 10.1071/ RD05022
26. Wang C, Cui Y-G, Wang X-H, Jia Y, Sinha Hikim A, et al. (2007) Transient Scrotal Hyperthermia and Levonorgestrel Enhance Testosterone-Induced Spermatogenesis Suppression in Men through Increased Germ Cell Apoptosis. The Journal of Clinical Endocrinology & Metabolism 92: 3292-3304. doi: 10.1210/jc.2007-0367
27. Cameron RD, Blackshaw AW (1980) The effect of elevated ambient temperature on spermatogenesis in the boar. J Reprod Fertil 59: 173-179.
28. Conine CC, Batista PJ, Gu W, Claycomb JM, Chaves DA, et al. (2010) Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26GRNAs and thermotolerant sperm in Caenorhabditis elegans. Proceedings of the National Academy of Sciences 107: 3588-3593. doi: 10.1073/pnas.0911685107
29. Bilgir C, Dombecki CR, Chen PF, Villeneuve AM, Nabeshima K (2013) Assembly of the Synaptonemal Complex is a Highly Temperature-Sensitive Process that is Supported by PGL-1 during Caenorhabditis elegans Meiosis. G3 (Bethesda). doi: 10.1534/g3.112.005165
30. Kawasaki I, Shim YH, Kirchner J, Kaminker J, Wood WB, et al. (1998) PGL-1, a predicted RNA-binding component of germ granules, is essential for fertility in C. elegans. Cell 94: 635-645.
31. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
32. Ihaka R, Gentleman R (2014) R: A Language for Data Analysis and Graphics. Journal of Computational and Graphical Statistics 5: 299-314. doi: 10.1080/ 10618600.1996.10474713