Skip to content
BY-NC-ND 4.0 license Open Access Published by De Gruyter Open Access December 13, 2018

Wing morphology in migratory North American monarchs: characterizing sources of variation and understanding changes through time

  • Micah G. Freedman EMAIL logo and Hugh Dingle
From the journal Animal Migration

Abstract

Monarch butterfly wing morphology varies substantially throughout their global range, both between resident and migratory populations and also within the migratory North American population. Here, we use a dataset comprising more than 1800 North American individuals collected between 1878-2017 to characterize the factors shaping continent-wide patterns of wing morphological variation. North American overwintering butterflies have forewings that are approximately 4.4% larger than those collected in summer breeding areas. Monarchs overwintering in Mexico have forewings that are approximately 1.8% larger than monarchs overwintering in California, conducive to the idea that migration distance is positively correlated with wing area. We find evidence for a latitudinal cline within North America, such that butterflies collected at higher latitudes have significantly larger and more elongated forewings. We also find a significant increase of approximately 4.9% in forewing area between 1878-2017, but no difference through time in wing elongation. This result is corroborated by a reanalysis of a recently published dataset of more than 600 butterflies from Mexican overwintering sites. We discuss possible reasons for this increase in wing size through time, including northward shifts in the monarch’s breeding range and changes in relative abundance of milkweed hosts, and present experimental data addressing the influence of larval host plant on adult wing morphology. Our analysis suggests that (1) migration is indeed an important selective force for monarch wing morphology; (2) wing size has increased through time in North America; (3) factors such as host plant identity must be considered to fully understand monarch wing morphological variation.

References

[1] Herman, W.S., Hormonally mediated events in adult monarch butterflies. In Rankin, M.A. (ed.), Migration: Mechanisms and Adaptive Significance, Contrib. Mar. Sci. 1985, 27, 799-815.Search in Google Scholar

[2] Dingle, H., Migration: The Biology of Life on the Move, 2nd edition, Oxford University Press, Oxford, United Kingdom, 2014.10.1093/acprof:oso/9780199640386.001.0001Search in Google Scholar

[3] Assumpcao L. et al., The use of morphometric analysis to predict the swimming efficiency of two Neotropical long-distance migratory species in fish passage, Neotrop. Ichthyol., 2012, 10, 797-804.10.1590/S1679-62252012000400012Search in Google Scholar

[4] Chapman, B.B. et al., Shape up or ship out: migratory behaviour predicts morphology across spatial scale in a freshwater fish, J. Anim. Ecol., 2015, 84, 1187-1193.10.1111/1365-2656.12374Search in Google Scholar PubMed

[5] Winkler, H. and Leisler, B., To be a migrant: Ecomorphological burdens and chances. In Greenberg, R. & Marra, P. (eds.). Birds of Two Worlds: the Ecology and Evolution of Migration, pp. 79-86. Johns Hopkins University Press, Baltimore, MD, 2005.Search in Google Scholar

[6] Bowlin, M.S. and Wikelski, M., Pointed wings, low wing loading and calm air reduce migratory flight costs in songbirds, PLoS One, 2008, 3, e2154.10.1371/journal.pone.0002154Search in Google Scholar PubMed PubMed Central

[7] Dingle, H. et al., Variation in body size and flight performance in milkweed bugs (Oncopeltus), Evolution 1980, 34, 371-385.10.1111/j.1558-5646.1980.tb04825.xSearch in Google Scholar PubMed

[8] Altizer, S. and Davis, A.K., Populations of Monarch butterflies with different migratory behaviors show divergence in wing morphology, Evolution, 2010, 64, 1018-1028.10.1111/j.1558-5646.2010.00946.xSearch in Google Scholar PubMed

[9] Beall, G. and Williams, C.B., Geographical variation in the wing length of Danaus plexippus (Lep. Rhopalocera), Proceedings of the Royal Entomological Society of London 1945, 20, 65-76.10.1111/j.1365-3032.1945.tb01068.xSearch in Google Scholar

[10] Dockx, C., Directional and stabilizing selection on wing size and shape in migrant and resident monarch butterflies, Danaus plexippus (L.), in Cuba, Biol. J. Linn. Soc., 2007, 92, 605-616.10.1111/j.1095-8312.2007.00886.xSearch in Google Scholar

[11] Li, Y. et al., Variation in forewing size linked to migratory status in monarch butterflies, Animal Migration, 2016, 3, 27-34.10.1515/ami-2016-0003Search in Google Scholar

[12] Gibo, D.L. and McCurdy, J.A., Lipid accumulation by migrating monarch butterflies (Danaus plexippus L.)., Can. J. Zool., 1973, 71, 76-82.10.1139/z93-012Search in Google Scholar

[13] Davis, A.K., Wing color of monarch butterflies (Danaus plexippus) in eastern North America across life stages: Migrants Are “redder” than breeding and overwintering stages, Psyche, 2009, Article ID 705780.10.1155/2009/705780Search in Google Scholar

[14] Hanley, D. et al., Forewing pigmentation predicts migration distance in wild-caught migratory monarch butterflies, Behav. Ecol., 2013, 24, 1108-1113.10.1093/beheco/art037Search in Google Scholar

[15] Satterfield, D.A. and Davis, A.K., Variation in wing characteristics of monarch butterflies during migration: Earlier migrants have redder and more elongated wings, Animal Migration, 2014, 2, 1-7.10.2478/ami-2014-0001Search in Google Scholar

[16] Yang, L.H. et al., Intra-population variation in the natal origins and wing morphology of overwintering western monarch butterflies Danaus plexippus, Ecography, 2016, 39, 998-1007.10.1111/ecog.01994Search in Google Scholar

[17] Flockhart, D.T.T. et al., Migration distance as a selective episode for wing morphology in a migratory insect., Mov Ecol, 2017, 5:7.10.1186/s40462-017-0098-9Search in Google Scholar PubMed PubMed Central

[18] Pocius, V.M. et al., Milkweed matters: Monarch butterfly (Lepidoptera: Nymphalidae) survival and development on nine Midwestern milkweed species, Environ. Entomol., 2017, 46, 1098-1105.10.1093/ee/nvx137Search in Google Scholar PubMed PubMed Central

[19] Freedman, M.G. et al., Non-migratory monarch butterflies, Danaus plexippus (L.), retain developmental plasticity and a navigational mechanism associated with migration, Biol. J. Linn. Soc., 2018, 123, 265-278.10.1093/biolinnean/blx148Search in Google Scholar

[20] Schneider, C.A. et al., NIH Image to ImageJ: 25 years of image analysis, Nat. Methods, 2012, 9, 671-675.10.1038/nmeth.2089Search in Google Scholar PubMed PubMed Central

[21] Kahle, D. and Wickham, H., ggmap: Spatial visualization with ggplot2. The R Journal, 2013, 5, 144-161.10.32614/RJ-2013-014Search in Google Scholar

[22] Bates, D. et al., Fitting linear mixed-effects models using lme4, Journal of Statistical Software, 2015, 67: 1-48.10.18637/jss.v067.i01Search in Google Scholar

[23] R Core Team. R: A language and environment for statistical computing, 2013, R Foundation for Statistical Computing, Vienna, Austria.Search in Google Scholar

[24] Ward M., Johnson S.D., Zalucki M.P., Modes of reproduction in three invasive milkweeds are consistent with Baker’s Rule, Biol. Invasions, 2012, 14, 1237-125010.1007/s10530-011-0152-2Search in Google Scholar

[25] Goyder D.J., Nicholas A., A revision of Gomphocarpus R. Br (Apocynaceae: Asclepiadeae), Kew Bull., 2001, 56, 769-836.10.2307/4119297Search in Google Scholar

[26] Davis, A.K. et al., Wing color predicts future mating success in male monarch butterflies, Ann. Entomol. Soc. Am., 2007, 100, 339-344.10.1603/0013-8746(2007)100[339:WCPFMS]2.0.CO;2Search in Google Scholar

[27] Solensky, M.J. and Oberhauser, K.S. Sperm precedence in monarch butterflies (Danaus plexippus), Behav. Ecol., 2009, 20, 328-334.10.1093/beheco/arp003Search in Google Scholar

[28] Hill H.F., Wenner A.M., Wells P.H., Reproductive behavior in an overwintering aggregation of monarch butterflies, Am. Midl. Nat., 1976, 95, 10-19.10.2307/2424229Search in Google Scholar

[29] Steffy G., Trends observed in fall migrant monarch butterflies (Lepidoptera: Nymphalidae) east of the Appalachian Mountains at an inland stopover in southern Pennsylvania over an eighteen year period, Ann. Entomol. Soc. Am., 2015, 108, 718-728.10.1093/aesa/sav046Search in Google Scholar

[30] Davis, A.K. and Rendon-Salinas, E., Are female monarch butterflies declining in eastern North America? Evidence of a 30-year change in sex ratios at Mexican overwintering sites, Biol. Lett., 2015, 6, 45-47.10.1098/rsbl.2009.0632Search in Google Scholar

[31] York, H.A. and Oberhauser, K.S, Effects of duration and timing of heat stress on monarch butterfly (Danaus plexippus) (Lepidoptera: Nymphalidae) development, J. Kans. Entomol. Soc., 2002, 75, 290-298.Search in Google Scholar

[32] Lyons, J.I. et al., Lack of genetic differentiation between monarch butterflies with divergent migration destinations, Mol. Ecol., 2002, 21, 3433-3444.10.1111/j.1365-294X.2012.05613.xSearch in Google Scholar

[33] Pierce, A.A. et al., Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies, Proc. Roy. Soc. B, 2014, 281, 20142230.10.1098/rspb.2014.2230Search in Google Scholar

[34] Dingle, H. et al., Distribution of the monarch butterfly, Danaus plexippus (L.)(Lepidoptera: Nymphalidae), in western North America, Biol. J. Linn. Soc., 2005, 85, 491-500.10.1111/j.1095-8312.2005.00512.xSearch in Google Scholar

[35] Atkinson, D., Temperature and organism size: a biological law for ectotherms? Adv. Ecol. Res., 1994, 25, 1-58.10.1016/S0065-2504(08)60212-3Search in Google Scholar

[36] Kingsolver, J.G. and Huey, R.B., Size, temperature, and fitness: three rules. - Evol. Ecol. Res., 2008, 10, 251-268.Search in Google Scholar

[37] Bradley, C.A. and Altizer, S., Parasites hinder monarch butterfly flight: implications for disease spread in migratory hosts, Ecol. Lett., 2005, 8, 290-300.10.1111/j.1461-0248.2005.00722.xSearch in Google Scholar

[38] Davis, A.K. et al., The redder the better: wing color predicts flight performance in monarch butterflies, PLoS One, 2012, 7, e41323.10.1371/journal.pone.0041323Search in Google Scholar

[39] Zhan, S. et al., The genetics of monarch butterfly migration and warning colouration, Nature, 2014, 514, 317-321.10.1038/nature13812Search in Google Scholar

[40] Pfeiler, E. et al., Population genetics of overwintering monarch butterflies, Danaus plexippus (Linnaeus), from central Mexico inferred from mitochondrial DNA and microsatellite markers, J. Hered. 2017, 108, 163-175.Search in Google Scholar

[41] Flockhart, D.T.T. et al., Regional climate on the breeding grounds predicts variation in the natal origin of monarch butterflies overwintering in Mexico over 38 years, Glob. Chang. Biol., 2017, 23, 2565-2576.10.1111/gcb.13589Search in Google Scholar

[42] Batalden R.V., Oberhauser K., Peterson A.T., Ecological niches in sequential generations of eastern North American monarch butterflies (Lepidoptera: Danaidae): The ecology of migration and likely climate change implications, Environ. Entomol., 2007, 36, 1365-1373.10.1603/0046-225X(2007)36[1365:ENISGO]2.0.CO;2Search in Google Scholar

[43] Howard, E., and Davis, A.K. 2015. Tracking the fall migration of eastern monarchs with Journey North roost sightings: New findings about the pace of fall migration, pp. 207-214. In K. Oberhauser, S. Altizer and K. Nail (eds.), Monarchs in a changing world: Biology and conservation of an iconic insect. Cornell University Press, Ithaca, NY.Search in Google Scholar

[44] Pleasants, J.M. and Oberhauser, K.S., Milkweed loss in agricultural fields because of herbicide use: effect on the monarch butterfly population, Insect Conserv. Divers., 2013, 6, 135-144.10.1111/j.1752-4598.2012.00196.xSearch in Google Scholar

[45] Zaya, D.N. et al., Long-term trends in Midwestern milkweed abundances and their relevance to monarch butterfly declines, Bioscience, 2017, 67, 343-356.10.1093/biosci/biw186Search in Google Scholar

[46] Boyle, J.H., Dalgleish, H.J. and Puzey, J. Monarch butterfly and milkweed declines substantially predate the use of genetically modified crops, BioRxiv preprint, 2018, https://doi.org/10.1101/378299.10.1101/378299Search in Google Scholar

[47] Zalucki M.P., Temperature and rate of development in Danaus plexippus L. and D. chrysippus L. (Lepidoptera: Nymphalidae), Aust. J. Entomol., 1982, 21, 241-24610.1111/j.1440-6055.1982.tb01803.xSearch in Google Scholar

[48] Malcolm, S.B. et al., Monarch butterfly voltinism: Effects of temperature constraints at different latitudes, Oikos, 1987, 49, 77-82.10.2307/3565556Search in Google Scholar

[49] Zalucki M.P. and Rochester W.A., Spatial and temporal population dynamics of monarchs down‐under: lessons for North America. In: The Monarch Butterfly: Biology and Conservation (eds K Oberhauser & M Solensky), pp. 219-228. Cornell University Press, Ithaca, USA, 2004.Search in Google Scholar

[50] Woodson, R.E., The North American species of Asclepias L., Ann. Mo. Bot. Gard., 1954, 41, 1-211.10.2307/2394652Search in Google Scholar

[51] Johnson, H. et al., Does skipping a meal matter to a butterfly’s appearance? Effects of larval food stress on wing morphology and color in monarch butterflies, PLoS One, 2014, 9, e93492.10.1371/journal.pone.0093492Search in Google Scholar

[52] Flockhart D.T.T., et. al., Tracking multi-generational colonization of the breeding grounds by monarch butterflies in eastern North America, Proc. Roy. Soc. B., 2013, 280, 20131087.10.1098/rspb.2013.1087Search in Google Scholar

[53] Suarez, A. and Tsutsui, N.D. The value of museum collections for research and society. Bioscience, 2005, 54, 66-74.10.1641/0006-3568(2004)054[0066:TVOMCF]2.0.CO;2Search in Google Scholar

[54] Holmes, M.W. et al., Natural history collections as windows on evolutionary processes, Mol. Ecol., 2016, 25: 864-881.10.1111/mec.13529Search in Google Scholar

[55] Fox, J. & S. Weisberg, An ‘R’ companion to applied regression, 2nd edition. Sage Publishing, Thousand Oaks, CA, 2011.Search in Google Scholar

Received: 2018-06-15
Accepted: 2018-09-20
Published Online: 2018-12-13
Published in Print: 2018-12-01

© by Micah G. Freedman, Hugh Dingle, published by De Gruyter

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

Downloaded on 3.6.2023 from https://www.degruyter.com/document/doi/10.1515/ami-2018-0003/html
Scroll to top button