Abstract
Monarch butterflies and their unique system of multigenerational migration have long fascinated the public, and concerns for the fate of this charismatic insect have grown due to the consistent declines in overwintering colony size over the last 20 years. Risks to this migratory insect have been considered in terms of climate change, habitat and thus population fragmentation, and decreased host plant availability. However, another obvious danger, that of decreased heterozygosity resulting from decreasing population size, has yet to be explored. Here we report experimental evidence for immediate inbreeding depression in individuals from the migratory population. Inbred matings produced less viable eggs and inbred offspring had higher developmental mortality and shorter lifespans. We discuss these results in the context of monarch migration extinction risk and suggest that additional genetic monitoring should be undertaken to protect this iconic animal.
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References
Altizer SM (2001) Migratory behaviour and host–parasite co-evolution in natural populations of monarch butterflies infected with a protozoan parasite. Evolut Ecol Res 3:567–581
Altizer S, Hobson KA, Davis AK, de Roode JC, Wassenaar LI (2015) Do healthy monarchs migrate farther? Tracking Natal origins of parasitized versus uninfected Monarch butterflies overwintering in Mexico. PLoS One 10:e0141371
Bartel RA, Oberhauser KS, de Roode JC, Altizer SM (2011) Monarch butterfly migration and parasite transmission in eastern North America. Ecology 92:342–51
Bates D, Maechler M, Bolker B, Walker S (2014). Lme4: linear mixed-effects models using S4 classes. R package version 1.1-6. http://cran.r-project.org/package=lme4
Brower LP, Pyle RM (2004) The interchange of migratory monarchs between Mexico and the western United States, and the importance of floral corridors to the fall and spring migrations. Conservation of migratory pollinators and their nectar corridors in North America. Arizona-Sonora Desert Museum, Natural History of the Sonoran Desert Region, pp 144–166
Brower LP, Calvert WH, Hedrick LE, Christian J (1977) Biological observations on an overwintering colony of monarch butterflies (Danaus plexippus, Danaidae) in Mexico. J Lepidopterists’ Soc 31:232–241
Brower LP, Kust DR, Rendon-Salinas E, Serrano EG, Kust KR, Miller J, Fernandez del Rey C, Pape K (2004) Catastrophic winter storm mortality of monarch butterflies in Mexico during January 2002. The Monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 151–166
Brower LP, Taylor OR, Williams EH, Slayback DA, Zubieta RR, Ramír ez MI (2012) Decline of monarch butterflies overwintering in Mexico: is the migratory phenomenon at risk? Insect Conserv Divers 5:95–100. doi:10.1111/j.1752-4598.2011.00142.x
Calvert WH (2004) Two methods of estimating overwintering monarch population size in Mexico. In: Oberhauser KS, Solensky MJ (eds) The Monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 121–128
Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358
de Roode JC, Gold LR, Altizer S (2007) Virulence determinants in a natural butterfly-parasite system. Parasitology 134:657–668. doi:10.1017/S0031182006002009
de Roode JC, Yates AJ, Altizer S (2008) Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. PNAS 105:7489–7494
de Roode JC, Chi J, Rarick RM, Altizer S (2009) Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (Danaus plexippus). Oecologia 161:67–75
Drayton JM, Jennions MD (2011) Inbreeding and measures of immune function in the cricket Teleogryllus commodus. Behav Ecol 22:486–492
Fox CW, Scheibly KL, Reed DH (2008) Experimental evolution of the genetic load and its implications for the genetic basis of inbreeding depression. Evolution 62:2236–2249
Flockhart DTT, Pichancourt JB, Norris DR, Martin TG (2014) Unravelling the annual cycle in a migratory animal: breeding-season habitat loss drives population declines of monarch butterflies. J Anim Ecol 84:155–165
Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of species extinction. Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland (Mass.), pp 19–34
Giuliano WM, Accamando AK, McAdams EJ (2004) Lepidoptera–habitat relationships in urban parks. Urban Ecosyst 7:361–370
Haikola S, Fortelius W, O’Hara RB, Kuussaari M, Wahlberg N, Saccheri IJ, Singer MC, Hanski I (2001) Inbreeding depression and the maintenance of genetic load in Melitaea cinxia metapopulations. Conserv Genet 2:325–335
Hall RJ, Altizer S, Bartel RA (2014) Greater migratory propensity in hosts lowers pathogen transmission and impacts. J Anim Ecol 83:1068–1077
Hedrick PW (1994) Purging inbreeding depression and the probability of extinction: full-sib mating. Heredity 73:363–372
Hill Jr. HF, Wenner AM, Wells PH (1976) Reproductive behavior in an overwintering aggregation of Monarch butterflies. American Midland Naturalist 95:10–19. http://www.jstor.org/stable/2424229
Howard E, Davis AK (2004) Documenting the spring movements of monarch butterflies with Journey North, a citizen science program. In: Oberhauser KS, Solensky MJ (eds) The Monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 105–116
Hughes PR, Radke CD, Renwick AA (1993) A simple, low-input method for continuous laboratory rearing of the monarch butterfly (Lepidoptera: Danaidae) for research. Am Entomol 39:109–111
Jeanpierre B, Oberhauser K, Freeman C (2005) Characteristics of professional development that effect change in secondary science teachers’ classroom practices. J Res Sci Teach 42:668–690
Kimura M, Maruyama T, Crow JF (1963) The mutation load in small populations. Genetics 48:1303
Lynch M, Gabriel W (1990) Mutation load and the survival of small populations. Evolution 44:1725–1737
Lyons JI, Pierce AA, Barribeau SM, Sternberg ED, Mongue AJ, de Roode JC (2012) Lack of genetic differentiation between monarch butterflies with divergent migration destinations. Mol Ecol 21:3433–3444
Malcolm SB (1993) Conservation of monarch butterfly migration in North America: an endangered phenomenon. Biol Conserv Monarch Butterfly 38:357
McLaughlin RE, Myers J (1970) Ophryocystis elektroscirrha sp. n., a Neogregarine Pathogen of the Monarch Butterfly Danaus plexippus (L.) and the Florida Queen Butterfly D. gilippus berenice Cramer. J Protozool 17:300–305. doi:10.1111/j.1550-7408.1970.tb02375.x
Mongue AJ, Ahmad MA, Tsai MV, de Roode JC (2014) Testing for cryptic female choice in monarch butterflies. Behav Ecol 26:386–395
Morris GM, Kline C, Morris SM (2015) Status of Danaus plexippus population in Arizona. J Lepidopterists’ Soc 69:91–107
Nieminen M, Singer MC, Fortelius W, Schöps K, Hanski I (2001) Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations. Am Nat 157:237–244
Pierce AA, Zalucki MP, Bangura M, Udawatta M, Kronforst MR, Altizer S, Haeger JF, de Roode JC (2014) Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies. Proc R Soc B Biol Sci 281:20142230. doi:10.1098/rspb.2014.2230
R Development Core Team R. 2011. R: a language and environment for statistical computing. R Foundation for Statistical Computing. http://www.r-project.org
Rantala MJ, Viitaniemi H, Roff DA (2011) Effects of inbreeding on potential and realized immune responses in Tenebrio molitor. Parasitology 138:906–912
Reid JM, Arcese P, Keller LF (2003) Inbreeding depresses immune response in song sparrows (Melospiza melodia): direct and inter-generational effects. Proc Biol Sci 270:2151–2157
Saccheri IJ, Brakefield PM, Nichols RA (1996) Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 2000–2013
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494
Saccheri IJ, Brakefield PM, Nichols RA (2014) Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50:2000–2013
Satterfield DA, Maerz JC, Altizer S (2015) Loss of migratory behaviour increases infection risk for a butterfly host. Proc R Soc B Biol Sci 282
Urquhart FA (1976) Found at last—Monarchs winter home. National Geographic 150:161–173
Urquhart FA, Urquhart NR (1978) Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico. Can J Zool 56:1759–1764
Vane-Wright RI (1993) The Columbus hypothesis: an explanation for the dramatic 19th century range expansion of the monarch butterfly. Biol Conserv Monarch Butterfly 38:179
Vidal O, Rendón-salinas E (2014) Dynamics and trends of overwintering colonies of the monarch butterfly in Mexico. Biol Conserv 180:165–175. doi:10.1016/j.biocon.2014.09.041
Vidal O, López-García J, Rendón-Salinas E (2014) Trends in Deforestation and forest degradation after a decade of monitoring in the Monarch Butterfly biosphere reserve in Mexico. Conserv Biol 28:177–186
Wassenaar LI, Hobson A (1998) Natal origins of migratory monarch butterflies at wintering colonies in Mexico: new isotopic evidence. Proc Natl Acad Sci USA 95:15436–15439
Zalucki MP, Clarke AR (2004) Monarchs across the Pacific: the Columbus hypothesis revisited. Biol J Linn Soc 82:111–121
Zalucki MP, Kitching RL (1982) The analysis and description of movement in adult Danaus plexippus L. (Lepidoptera: Danainae). Behaviour 80:174–198
Zhan S, Zhang W, Niitepõld K, Hsu J, Haeger JF, Zalucki MP, Altizer S, de Roode JC, Reppert SM, Kronforst MR (2014) The genetics of monarch butterfly migration and warning colouration. Nature 514:317–321
Acknowledgments
We thank the de Roode lab for logistical and theoretical help with this project; R.D. Holt and M. Barfield for comments on the manuscript; and C. Chaffee and A. Gonzalez Rodriguez for discussion. This work was supported by National Science Foundation grant DEB-1257160 to J.C.D.R.
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Mongue, A.J., Tsai, M.V., Wayne, M.L. et al. Inbreeding depression in monarch butterflies. J Insect Conserv 20, 477–483 (2016). https://doi.org/10.1007/s10841-016-9880-z
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DOI: https://doi.org/10.1007/s10841-016-9880-z