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Research Article

Evidence for inter-population variation in waiting times in a self-fertilizing flatworm

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Pages 158-168 | Received 03 Dec 2019, Accepted 16 Feb 2020, Published online: 23 Feb 2020

References

  • Arunkumar R, Ness RW, Wright SI, Barrett SCH. 2015. The evolution of selfing is accompanied by reduced efficacy of selection and purging of deleterious mutations. Genetics. 199(3):817–829. doi:10.1534/genetics.114.172809.
  • Barrett SCH, Charlesworth D. 1991. Effects of a change in the level of inbreeding on the genetic load. Nature. 352(6335):522–524. doi:10.1038/352522a0.
  • Brunet J. 1992. Sex allocation in hermaphroditic plants. Trends Ecol Evol. 7(3):79–84. doi:10.1016/0169-5347(92)90245-7.
  • Busch JW, Delph LF. 2012. The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Ann Bot. 109(3):553–562. doi:10.1093/aob/mcr219.
  • Charlesworth D, Charlesworth B. 1979. The evolutionary genetics of sexual systems in flowering plants. Proc R Soc B. 205(1161):513–530. doi:10.1098/rspb.1979.0082.
  • Charlesworth D, Charlesworth B. 1987. Inbreding depression and its evolutionary consequences. Annu Rev Ecol Syst. 18(1):237–268. doi:10.1146/annurev.es.18.110187.001321.
  • Charlesworth D, Willis JH. 2009. The genetics of inbreeding depression. Nat Rev Genet. 10(11):783–796. doi:10.1038/nrg2664.
  • Charnov EL. 1982. The theory of sex allocation. Princeton University Press. Princeton NJ.
  • Damgaard C, Loeschcke V. 1994. Genetic variation for selfing rate and the dependence of selfing rate on mating history in Brassica napus (rape seed). Heredity. 72(6):570–573. doi:10.1038/hdy.1994.78.
  • Darwin C. 1987. The effects of cross and self-fertilization in the vegetable kingdom. London: J. Murray.
  • De Groot GA, Verduyn B, Wubs ERJ, Erkens RHJ, During HJ. 2012. Inter-and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing. BMC Plant Biol. 12:3.
  • De Visser JAGM, Ter Maat A, Zonneveld C. 1994. Energy budgets and reproductive allocation in the simultaneous hermaphrodite pond snail, Lymnaea stagnalis (L.): a trade-off between male and female function. Am Nat. 144(5):861–867. doi:10.1086/285712.
  • Dorken ME, Pannell JR. 2009. Hermaphroditic sex allocation evolves when mating opportunities change. Curr Biol. 19(6):514–517. doi:10.1016/j.cub.2009.01.067.
  • Escobar JS, Auld JR, Correa AC, Alonso JM, Bony YK, Coutellec MA, Koene JM, Pointier J-P, Jarne P, David P. 2011. Patterns of mating-system evolution in hermaphroditic animals: correlations among selfing rate, inbreeding depression, and the timing of reproduction. Evolution. 65(5):1233–1253. doi:10.1111/j.1558-5646.2011.01218.x.
  • Escobar JS, Epinat G, Sarda V, David P. 2007. No correlation between inbreeding depression and delayed selfing in the freshwater snail Physa acuta. Evolution. 61(11):2655–2670. doi:10.1111/j.1558-5646.2007.00223.x.
  • Escobar JS, Facon B, Jarne P, Goudet J, David P. 2009. Correlated evolution of mating strategy and inbreeding depression within and among populations of the hermaphroditic snail Physa acuta. Evolution 63(11):2790–2804. doi:10.1111/j.1558-5646.2009.00760.x.
  • Fisher RA. 1941. Average excess and average effect of a gene substitution. Annalytics Eugenics. 11(1):53–63. doi:10.1111/j.1469-1809.1941.tb02272.x.
  • Giannakara A, Ramm SA. 2017. Self-fertilization, sex allocation and spermatogenesis kinetics in the hypodermically inseminating flatworm Macrostomum pusillum. J Exp Biol. 220(9):1568–1577. doi:10.1242/jeb.149682.
  • Giannakara A, Schärer L, Ramm SA. 2016. Sperm competition-induced plasticity in the speed of spermatogenesis. BMC Evol Biol. 16:60.
  • Goodwillie C, Kalisz S, Eckert CG. 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations and empirical evidence. Annu Rev Ecol Evol Syst. 36(1):47–79. doi:10.1146/annurev.ecolsys.36.091704.175539.
  • Goodwillie C, Weber JJ. 2018. The best of both worlds? A review of delayed selfing in flowering plants. Am J Bot. 105(4):641–655. doi:10.1002/ajb2.1045.
  • Hart MK, Kratter AW, Svoboda A, Lawrence CL, Sargent CR, Crowley PH. 2010. Sex allocation in a group-living simultaneous hermaphrodite: effects of density at two different spatial scales. Evol Ecol Res. 12:189–202.
  • Husband BC, Schemske DW. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution. 50(1):54–70. doi:10.1111/j.1558-5646.1996.tb04472.x.
  • Janicke T, Marie-Orleach L, De Mulder K, Berezikov E, Ladurner P, Vizoso DB, Schärer L. 2013. Sex allocation adjustment to mating group size in a simultaneous hermaphrodite. Evolution. 67(11):3233–3242. doi:10.1111/evo.12189.
  • Janicke T, Sandner P, Ramm SA, Vizoso DB, Schärer L. 2016. Experimentally evolved and phenotypically plastic responses to enforced monogamy in a hermaphroditic flatworm. J Evol Biol. 29(9):1713–1727. doi:10.1111/jeb.12910.
  • Jarne P, Auld JR. 2006. Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution. 60(9):1816–1824. doi:10.1111/j.0014-3820.2006.tb00525.x.
  • Jarne P, Charlesworth D. 1993. The evolution of the selfing rate in functionally hermaphrodite plants and animals. Annu Rev Ecol Evol Syst. 24(1):441–466. doi:10.1146/annurev.es.24.110193.002301.
  • Jarne P, Finot L, Delay B, Thaler L. 1991. Self-fertilization versus cross-fertilization in the hermaphroditic freshwater snail Bulinus globosus. Evolution. 45(5):1136–1146. doi:10.2307/2409721.
  • Johnston MO, Das B, Hoeh WR. 1998. Negative correlation between male allocation and rate of self-fertilization in a hermaphroditic animal. Proc Natl Acad Sci. 95(2):617–620. doi:10.1073/pnas.95.2.617.
  • Kalisz S, Vogler D, Fails B, Finer M, Shepard E, Herman T, Gonzales R. 1999. The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae). Am J Bot. 86(9):1239–1247. doi:10.2307/2656771.
  • Ladurner P, Schärer L, Salvenmoser W, Rieger RM. 2005. A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes: Macrostomum lignano, n.sp. (Rhabditophora, Macrostomorpha). J Zool Syst Evol Res. 43(2):114–126. doi:10.1111/j.1439-0469.2005.00299.x.
  • Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution. 39(1):24–40. doi:10.1111/j.1558-5646.1985.tb04077.x.
  • Lande R, Schemske DW, Schultz ST. 1994. High inbreeding depression, selective interference among loci and the threshold selfing rate for purging recessive lethal mutations. Evolution. 48(4):965–978. doi:10.1111/j.1558-5646.1994.tb05286.x.
  • Lloyd DG, Schoen DJ. 1992. Self- and cross-fertilization in plants. I. Functional dimensions. Int J Plant Sci. 153(3, Part 1):358–369. doi:10.1086/297040.
  • Lorenzi MC, Sella G, Schleicherova D, Ramella L. 2005. Outcrossing hermaphroditic polychaete worms adjust their sex allocation to social conditions. J Evol Biol. 18(5):1341–1347. doi:10.1111/j.1420-9101.2005.00916.x.
  • Mousset M, David P, Petit C, Pouzadoux J, Hatt C, Flaven É, Ronce O, Mignot A. 2016. Lower selfing rates in metallicolous populations than in non-metallicolous populations of the pseudometallophyte Noccaea caerulescens (Brassicaceae) in Southern France. Ann Bot. 117(3):507–519. doi:10.1093/aob/mcv191.
  • Noël E, Chemtob Y, Janicke T, Sarda V, Pélissié B, Jarne P, David P. 2016. Reduced mate availability leads to evolution of self-fertilization and purging of inbreeding depression in a hermaphrodite. Evolution. 70(3):625–640. doi:10.1111/evo.12886.
  • Porcher E, Lande R. 2016. Inbreeding depression under mixed outcrossing, self-fertilization and sib-mating. BMC Evol Biol. 16(1):105. doi:10.1186/s12862-016-0668-2.
  • Puurtinen M, Emily Knott K, Suonpää S, Nissinen K, Kaitala V. 2007. Predominance of outcrossing in Lymnaea stagnalis despite low apparent fitness costs of self-fertilization. J Evol Biol. 20(3):901–912. doi:10.1111/j.1420-9101.2007.01312.x.
  • R: A language and environment for statistical analysis. 2011. R Development Core Team.
  • Ramm SA, Lengerer B, Arbore R, Pjeta R, Wunderer J, Giannakara A, Berezikov E, Ladurner P, Schärer L. 2019. Sex allocation plasticity on a transcriptome scale: socially sensitive gene expression in a simultaneous hermaphrodite. Mol Ecol. 28(9):2321–2341. doi:10.1111/mec.15077.
  • Ramm SA, Schlatter A, Poirier M, Schärer L. 2015. Hypodermic self-insemination as a reproductive assurance strategy. Proc R Soc London Ser B.282(1811):20150660.
  • Ramm SA, Vizoso DB, Schärer L. 2012. Occurrence, costs and heritability of delayed selfing in a free-living flatworm. J Evol Biol. 25(12):2559–2568. doi:10.1111/jeb.12012.
  • Roff DA. 2002. Inbreeding depression: tests of the overdominance and partial dominance hypotheses. Evolution. 56(4):768–775. doi:10.1111/j.0014-3820.2002.tb01387.x.
  • RStudio Team. 2015. RStudio: Integrating Development for RRStudio, Inc., Boston MA
  • Schärer L. 2009. Tests of sex allocation theory in simultaneously hermaphroditic animals. Evolution. 63(6):1377–1405. doi:10.1111/j.1558-5646.2009.00669.x.
  • Schärer L, Ladurner P. 2003. Phenotypically plastic adjustment of sex allocation in a simultaneous hermaphrodite. Proc R Soc London Ser B. 270(1518):935–941. doi:10.1098/rspb.2002.2323.
  • Schärer L, Littlewood DTJ, Waeschenbach A, Yoshida W, Vizoso DB. 2011. Mating behavior and the evolution of sperm design. Proc Natl Acad Sci. 108(4):1490–1495. doi:10.1073/pnas.1013892108.
  • Schärer L, Ramm SA. 2016. Hermaphrodites. In Kliman, R. (ed.) Encyclopedia of evolutionary biology. Oxford. Elsevier. Vol.2.  pp. 212–224.
  • Schärer L, Sandner P, Michiels NK. 2005. Trade-off between male and female allocation in the simultaneously hermaphroditic flatworm Macrostomum sp. J Evol Biol. 18(2):396–404. doi:10.1111/j.1420-9101.2004.00827.x.
  • Schemske DW, Lande R. 1985. The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution. 39(1):41–52. doi:10.1111/j.1558-5646.1985.tb04078.x.
  • Schjørring S. 2004. Delayed selfing in relation to the availability of a mating partner in the cestode Schistocephalus solidus. Evolution. 58(11):2591–2596. doi:10.1554/04-270.
  • Schjørring S, Jäger I. 2007. Incestuous mate preference by a simultaneous hermaphrodite with strong inbreeding depression. Evolution. 61(2):423–430. doi:10.1111/j.1558-5646.2007.00028.x.
  • Theologidis I, Chelo IM, Goy C, Teotónio H. 2014. Reproductive assurance drives transitions to self-fertilization in experimental Caenorhabditis elegans. BMC Biol. 12(1):93.
  • Trouvé S, Jourdane J, Renaud F, Durand P, Morand S. 1999. Adaptive sex allocation in a simultaneous hermaphrodite. Evolution. 53(5):1599–1604. doi:10.2307/2640905.
  • Tsitrone A, Duperron S, David P. 2003a. Delayed selfing as an optimal mating strategy in preferentially outcrossing species: theoretical analysis of the optimal age at first reproduction in relation to mate availability. Am Nat. 162(3):318–331. doi:10.1086/375542.
  • Tsitrone A, Jarne P, David P. 2003b. Delayed selfing and resource reallocations in relation to mate availability in the freshwater snail Physa acuta. Am Nat. 162(4):474–488. doi:10.1086/376889.
  • Whitehead MR, Lanfear R, Mitchell RJ, Karron JD. 2018. Plant mating systems often vary widely among populations. [Mini Review]. Front Ecol Evol. 6(38).
  • Winkler L, Ramm SA. 2018. Experimental evidence for reduced male allocation under selfing in a simultaneously hermaphroditic animal. Biol Lett. 14(10):20180570.

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