Natural selection by pollinators on floral attractive and defensive traits did not translate into selection via fruits in common milkweed

Authors

DOI:

https://doi.org/10.26786/1920-7603(2024)758

Keywords:

Asclepias syriaca, herbivory, latex, nectar concentration, male fitness, phenotypic selection

Abstract

Considering both pollinator and herbivore pressures on plant reproductive and defensive traits is key to understanding patterns of selection for plants. However, phenotypic selection studies connecting floral traits and plant defenses with pollinator activity and herbivore damage remain rare. We used the common milkweed, Asclepias syriaca (Apocynaceae), to study phenotypic selection on attractive and defensive traits, and nectar rewards. We measured herbivore (leaf damage) and pollinator activity (pollinia movement) and quantified selection via female (pollinia insertions and fruit number) and male fitness (pollinia removals). We found selection to increase plant and inflorescence size and to decrease floral size (i.e. petal width) via female fitness. We also detected selection to increase floral but not leaf latex. The lack of selection on leaf latex was congruent with the low herbivory observed, however we also did not observe florivory in the population that would explain the advantage of more floral latex. Interestingly, we found selection on attractive traits differed via pollinia insertions and fruits initiated, suggesting that something other than pollinators was driving selection via fruit production. In contrast to female fitness, we did not find selection on any trait through male fitness, suggesting no sexual conflicting selection, at least through these proxies. Our findings reinforce the importance of the direct assessment of pollinator pressures in phenotypic selection studies before assuming pollinators as drivers of floral evolution by natural selection. Further work in southern populations closer to the centre of the species range, where herbivory and plant defense investment are higher, may help elucidate selection on attractive and defensive traits.

Author Biography

Lucie Vézina, University of New Brunswick

Current address: Department of Integrative Biology, University of Guelph, Guelph, Ontario, Canada

References

Adler LS, Irwin RE (2005) Ecological costs and benefits of defenses in nectar. Ecology 86:2968-2978. https://doi.org/10.1890/05-0118 DOI: https://doi.org/10.1890/05-0118

Adler LS, Seifert MG, Wink M, Morse GE (2012) Reliance on pollinators predicts defensive chemistry across tobacco species. Ecology Letters 15:1140-1148. https://doi.org/10.1111/j.1461-0248.2012.01838.x DOI: https://doi.org/10.1111/j.1461-0248.2012.01838.x

Adler LS, Wink M, Distl M, Lentz AJ (2006) Leaf herbivory and nutrients increase nectar alkaloids. Ecology Letters 9:960-967. https://doi.org/10.1111/j.1461-0248.2006.00944.x DOI: https://doi.org/10.1111/j.1461-0248.2006.00944.x

Agrawal AA (2005) Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evolutionary Ecology Research 7:651-667.

Agrawal A (2017) Monarchs and milkweed: a migrating butterfly, a poisonous plant, and their remarkable story of coevolution. In: Monarchs and Milkweed. Princeton University Press https://doi.org/10.1515/9781400884766 DOI: https://doi.org/10.1515/9781400884766

Agrawal AA, Espinosa del Alba L, López-Goldar X, Hastings AP, White RA, Halitschke R, Dobler S, Petschenka G, Duplais C (2022) Functional evidence supports adaptive plant chemical defense along a geographical cline. Proceedings of the National Academy of Sciences 119:e2205073119. https://doi.org/10.1073/pnas.2205073119 DOI: https://doi.org/10.1073/pnas.2205073119

Agrawal AA, Lajeunesse MJ, Fishbein M (2008) Evolution of latex and its constituent defensive chemistry in milkweeds (Asclepias): a phylogenetic test of plant defense escalation. Entomologia Experimentalis et Applicata 128:126-138. https://doi.org/10.1111/j.1570-7458.2008.00690.x DOI: https://doi.org/10.1111/j.1570-7458.2008.00690.x

Agrawal AA, Patrick ET, Hastings AP (2014) Tests of the coupled expression of latex and cardenolide plant defense in common milkweed (Asclepias syriaca). Ecosphere 5:126. https://doi.org/10.1890/ES14-00161.1 DOI: https://doi.org/10.1890/ES14-00161.1

Ashman TL, Morgan MT (2004) Explaining phenotypic selection on plant attractive characters: male function, gender balance or ecological context? Proceedings of the Royal Society of London Series B: Biological Sciences 271:553-559. https://doi.org/10.1098/rspb.2003.2642 DOI: https://doi.org/10.1098/rspb.2003.2642

Austen EJ, Weis AE (2016) The causes of selection on flowering time through male fitness in a hermaphroditic annual plant. Evolution 70:111-125. https://doi.org/10.1111/evo.12823 DOI: https://doi.org/10.1111/evo.12823

Baker AM, Potter DA (2018) Japanese beetles' feeding on milkweed flowers may compromise efforts to restore monarch butterfly habitat. Scientific Reports 8:12139. https://doi.org/10.1038/s41598-018-30731-z DOI: https://doi.org/10.1038/s41598-018-30731-z

Bingham RA, Agrawal AA (2010) Specificity and trade-offs in the induced plant defence of common milkweed Asclepias syriaca to two lepidopteran herbivores. Journal of Ecology 98:1014-1022. https://doi.org/10.1111/j.1365-2745.2010.01681.x DOI: https://doi.org/10.1111/j.1365-2745.2010.01681.x

Birnbaum SSL, Abbot P (2018) Insect adaptations toward plant toxins in milkweed-herbivores systems - a review. Entomologia Experimentalis et Applicata 166:357-366. https://doi.org/10.1111/eea.12659 DOI: https://doi.org/10.1111/eea.12659

Briscoe Runquist RD, Geber MA, Pickett-Leonard M, Moeller DA (2017) Mating system evolution under strong pollen limitation: Evidence of disruptive selection through male and female fitness in Clarkia xantiana. The American Naturalist 189:549-563. https://doi.org/10.1086/691192 DOI: https://doi.org/10.1086/691192

Broyles SB, Wyatt R (1990) Paternity analysis in a natural population of Ascepias exaltata: multiple paternity, functional gender, and the "pollen-donation hypothesis." Evolution 44:1454-1468. https://doi.org/10.1111/j.1558-5646.1990.tb03838.x DOI: https://doi.org/10.1111/j.1558-5646.1990.tb03838.x

Bruinsma M, Lucas-Barbosa D, ten Broeke CJM, van Dam NM, van Beek TA, Dicke M, van Loon JJA (2014) Folivory affects composition of nectar, floral odor and modifies pollinator behavior. Journal of Chemical Ecology 40:39-49. https://doi.org/10.1007/s10886-013-0369-x DOI: https://doi.org/10.1007/s10886-013-0369-x

Burkle LA, Runyon JB (2016) Drought and leaf herbivory influence floral volatiles and pollinator attraction. Global Change Biology 22:1644-1654. https://doi.org/10.1111/gcb.13149 DOI: https://doi.org/10.1111/gcb.13149

Caruso CM, Eisen KE, Martin RA, Sletvold N (2019) A meta-analysis of the agents of selection on floral traits. Evolution 73:4-14. https://doi.org/10.1111/evo.13639 DOI: https://doi.org/10.1111/evo.13639

Caruso CM, Remington DLD, Ostergren KE (2005) Variation in resource limitation of plant reproduction influences natural selection on floral traits of Asclepias syriaca. Oecologia 146:68-76. https://doi.org/10.1007/s00442-005-0183-4 DOI: https://doi.org/10.1007/s00442-005-0183-4

Chapurlat E, Ågren J, Anderson J, Friberg M, Sletvold N (2019) Conflicting selection on floral scent emission in the orchid Gymnadenia conopsea. New Phytologist 222:2009-2022. https://doi.org/10.1111/nph.15747 DOI: https://doi.org/10.1111/nph.15747

Christopher DA, Mitchell RJ, Karron JD (2020) Pollination intensity and paternity in flowering plants. Annals of Botany 125:1-9. https://doi.org/10.1093/aob/mcz159 DOI: https://doi.org/10.1093/aob/mcz159

Conner JK, Rush S, Kercher S, Jennetten P (1996) Measurements of natural selection on floral traits in wild radish (Raphanus raphanistrum) II. Selection through lifetime male and total fitness. Evolution 50:1137-1146. https://doi.org/10.1111/j.1558-5646.1996.tb02354.x DOI: https://doi.org/10.1111/j.1558-5646.1996.tb02354.x

Egan PA, Muola A, Parachnowitsch AL, Stenberg JA (2021) Pollinators and herbivores interactively shape selection on strawberry defence and attraction. Evolution Letters 5:636-643. https://doi.org/10.1002/evl3.262 DOI: https://doi.org/10.1002/evl3.262

Fritz RS, Morse DH (1981) Nectar parasitism of Asclepias syriaca by ants: effect on nectar levels, pollinia insertion, pollinaria removal and pod production. Oecologia 50:316-319. https://doi.org/10.1007/BF00344969 DOI: https://doi.org/10.1007/BF00344969

Galil J, Zeroni M (1965) Nectar system of Asclepias curassavica. Botanical Gazette 126:144-148. https://doi.org/10.1086/336310 DOI: https://doi.org/10.1086/336310

Gustafson NW, Couture JJ, Dalgleish HJ (2023) Herbivory, plant traits and nectar chemistry interact to affect the community of insect visitors and pollination in common milkweed, Asclepias syriaca. Oecologia 201:91-105. https://doi.org/10.1007/s00442-022-05290-w DOI: https://doi.org/10.1007/s00442-022-05290-w

Harder LD, Johnson SD (2009) Darwin's beautiful contrivances: Evolutionary and functional evidence for floral adaptation. New Phytologist 183:530-545. https://doi.org/10.1111/j.1469-8137.2009.02914.x DOI: https://doi.org/10.1111/j.1469-8137.2009.02914.x

Hoffmeister M, Junker RR (2017) Herbivory-induced changes in the olfactory and visual display of flowers and extrafloral nectaries affect pollinator behavior. Evolutionary Ecology 31:269-284. https://doi.org/10.1007/s10682-016-9875-y DOI: https://doi.org/10.1007/s10682-016-9875-y

Howard AF, Barrows EM (2014) Self-pollination rate and floral-display size in Asclepias syriaca (common milkweed) with regard to floral-visitor taxa. BMC Evolutionary Biology 14:144. https://doi.org/10.1186/1471-2148-14-144 DOI: https://doi.org/10.1186/1471-2148-14-144

Jennersten O, Morse DH (1991) The quality of pollination by diurnal and nocturnal insects visiting common milkweed, Asclepias syriaca. The American Midland Naturalist 125:18-28. https://doi.org/10.2307/2426365 DOI: https://doi.org/10.2307/2426365

Jones PL, Agrawal AA (2016) Consequences of toxic secondary compounds in nectar for mutualist bees and antagonist butterflies. Ecology 97:2570-2579. https://doi.org/10.1002/ecy.1483 DOI: https://doi.org/10.1002/ecy.1483

Kessler A, Chautá A (2020) The ecological consequences of herbivore-induced plant responses on plant-pollinator interactions. Emerging Topics in Life Sciences 4:33-43. https://doi.org/10.1042/ETLS20190121 DOI: https://doi.org/10.1042/ETLS20190121

Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92:1769-1780. https://doi.org/10.1890/10-1945.1 DOI: https://doi.org/10.1890/10-1945.1

Kevan PG, Eisikowitch D, Rathwell B (1989) The role of nectar in the germination of pollen in Asclepias syriaca L. Botanical Gazette 150:266-270. https://doi.org/10.1086/337771 DOI: https://doi.org/10.1086/337771

Knauer AC, Schiestl FP (2017) The effect of pollinators and herbivores on selection for floral signals: a case study in Brassica rapa. Evolutionary Ecology 31:285-304. https://doi.org/10.1007/s10682-016-9878-8 DOI: https://doi.org/10.1007/s10682-016-9878-8

La Rosa RJ (2015) Floral evolution in milkweeds: evidence for selection past and present. Ph.D., Michigan State University, United States -- Michigan.

La Rosa RJ, Conner JK (2017) Floral function: effects of traits on pollinators, male and female pollination success, and female fitness across three species of milkweeds (Asclepias). American Journal of Botany 104:150-160. https://doi.org/10.3732/ajb.1600328 DOI: https://doi.org/10.3732/ajb.1600328

Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210. https://doi.org/10.2307/2408842 DOI: https://doi.org/10.2307/2408842

Lehtilä K, Strauss SY (1999) Effects of foliar herbivory on male and female reproductive traits of wild radish, Raphanus raphanistrum. Ecology 80:116-124. https://doi.org/10.1890/0012-9658(1999)080[0116:EOFHOM]2.0.CO;2 DOI: https://doi.org/10.1890/0012-9658(1999)080[0116:EOFHOM]2.0.CO;2

López-Goldar X, Hastings A, Züst T, Agrawal A (2022) Evidence for tissue-specific defence-offence interactions between milkweed and its community of specialized herbivores. Molecular Ecology 31:3254-3265. https://doi.org/10.1111/mec.16450 DOI: https://doi.org/10.1111/mec.16450

Maad J, Alexandersson R (2004) Variable selection in Platanthera bifolia (Orchidaceae): phenotypic selection differed between sex functions in a drought year. Journal of Evolutionary Biology 17:642-650. https://doi.org/10.1111/j.1420-9101.2004.00703.x DOI: https://doi.org/10.1111/j.1420-9101.2004.00703.x

Manson JS, Rasmann S, Halitschke R, Thomson JD, Agrawal AA (2012) Cardenolides in nectar may be more than a consequence of allocation to other plant parts: a phylogenetic study of Asclepias. Functional Ecology 26:1100-1110. https://doi.org/10.1111/j.1365-2435.2012.02039.x DOI: https://doi.org/10.1111/j.1365-2435.2012.02039.x

Matsumura S, Arlinghaus R, Dieckmann U (2012) Standardizing selection strengths to study selection in the wild: A critical comparison and suggestions for the future. BioScience 62:1039-1054. https://doi.org/10.1525/bio.2012.62.12.6 DOI: https://doi.org/10.1525/bio.2012.62.12.6

Matter SF, Landry JB, Greco AM, LaCourse CD (1999) Importance of floral phenology and florivory for Tetraopes tetraophthalmus (Coleoptera: Cerambycidae): tests at the population and Individual level. Environmental Entomology 28:1044-1051. https://doi.org/10.1093/ee/28.6.1044 DOI: https://doi.org/10.1093/ee/28.6.1044

Morgan MT, Schoen DJ (1997) Selection on reproductive characters: floral morphology in Asclepias syriaca. Heredity 79:433-441. https://doi.org/10.1038/hdy.1997.178 DOI: https://doi.org/10.1038/sj.hdy.6882040

Morse DH, Fritz RS (1983) Contributions of diurnal and nocturnal insects to the pollination of common milkweed (Asclepias syriaca L.) in a pollen-limited system. Oecologia 60:190-197. https://doi.org/10.1007/BF00379521 DOI: https://doi.org/10.1007/BF00379521

Opedal ØH (2021) A functional view reveals substantial predictability of pollinator-mediated selection. Journal of Pollination Ecology 30:273-288. https://doi.org/10.26786/1920-7603(2021)673 DOI: https://doi.org/10.26786/1920-7603(2021)673

Parachnowitsch AL, Caruso CM (2008) Predispersal seed herbivores, not pollinators, exert selection on floral traits via female fitness. Ecology 89:1802-1810. https://doi.org/10.1890/07-0555.1 DOI: https://doi.org/10.1890/07-0555.1

Parachnowitsch AL, Caruso CM, Campbell SA, Kessler A (2012) Lobelia siphilitica plants that escape herbivory in time also have reduced latex production. PLoS ONE 7:e37745. https://doi.org/10.1371/journal.pone.0037745 DOI: https://doi.org/10.1371/journal.pone.0037745

Parachnowitsch AL, Kessler A (2010) Pollinators exert natural selection on flower size and floral display in Penstemon digitalis. New Phytologist 188:393-402. https://doi.org/10.1111/j.1469-8137.2010.03410.x DOI: https://doi.org/10.1111/j.1469-8137.2010.03410.x

Parachnowitsch AL, Manson JS, Sletvold N (2019) Evolutionary ecology of nectar. Annals of Botany 123:247-261. https://doi.org/10.1093/aob/mcy132 DOI: https://doi.org/10.1093/aob/mcy132

Pleasants JM (1991) Evidence for short-distance dispersal of pollinia in Asclepias syriaca L. Functional Ecology 5:75-82. https://doi.org/10.2307/2389557 DOI: https://doi.org/10.2307/2389557

Pyke GH (2016) Floral Nectar: Pollinator attraction or manipulation? Trends in Ecology & Evolution 31:339-341. https://doi.org/10.1016/j.tree.2016.02.013 DOI: https://doi.org/10.1016/j.tree.2016.02.013

Raguso RA (2004) Why are some floral nectars scented? Ecology 85:1486-1494. https://doi.org/10.1890/03-0410 DOI: https://doi.org/10.1890/03-0410

Ramos SE, Schiestl FP (2019) Rapid plant evolution driven by the interaction of pollination and herbivory. Science 364:193-196. https://doi.org/10.1126/science.aav6962 DOI: https://doi.org/10.1126/science.aav6962

Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecology Letters 14:476-483. https://doi.org/10.1111/j.1461-0248.2011.01609.x DOI: https://doi.org/10.1111/j.1461-0248.2011.01609.x

Santangelo JS, Thompson KA, Johnson MTJ (2019) Herbivores and plant defences affect selection on plant reproductive traits more strongly than pollinators. Journal of Evolutionary Biology 32:4-18. https://doi.org/10.1111/jeb.13392 DOI: https://doi.org/10.1111/jeb.13392

Siepielski AM, Gotanda KM, Morrissey MB, Diamond SE, DiBattista JD, Carlson SM (2013) The spatial patterns of directional phenotypic selection. Ecology Letters 16:1382-1392. https://doi.org/10.1111/ele.12174 DOI: https://doi.org/10.1111/ele.12174

Siepielski AM, Morrissey MB, Buoro M, Carlson SM, Caruso CM, Clegg SM, Coulson T, DiBattista J, Gotanda KM, Francis CD, Hereford J, Kingsolver JG, Augustine KE, Kruuk LEB, Martin RA, Sheldon BC, Sletvold N, Svensson EI, Wade MJ, MacColl ADC (2017) Precipitation drives global variation in natural selection. Science 355:959-962. https://doi.org/10.1126/science.aag2773 DOI: https://doi.org/10.1126/science.aag2773

Sletvold N (2019) The context dependence of pollinator-mediated selection in natural populations. International Journal of Plant Sciences 180:934-943. https://doi.org/10.1086/705584 DOI: https://doi.org/10.1086/705584

Sletvold N, Grindeland JM, Ågren J (2010) Pollinator‐mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica. New Phytologist 188: 385-392 https://doi.org/10.1111/j.1469-8137.2010.03296.x DOI: https://doi.org/10.1111/j.1469-8137.2010.03296.x

Sletvold N, Moritz KK, Ågren J (2014) Additive effects of pollinators and herbivores result in both conflicting and reinforcing selection on floral traits. Ecology 96:214-221. https://doi.org/10.1890/14-0119.1 DOI: https://doi.org/10.1890/14-0119.1

Sletvold N, Trunschke J, Smit M, Verbeek J, Ågren J (2016) Strong pollinator‐mediated selection for increased flower brightness and contrast in a deceptive orchid. Evolution 70:716-724. https://doi.org/10.1111/evo.12881 DOI: https://doi.org/10.1111/evo.12881

Southwick EE (1983) Nectar biology and nectar feeders of common milkweed, Asclepias syriaca L. Bulletin of the Torrey Botanical Club 110:324. https://doi.org/10.2307/2996186 DOI: https://doi.org/10.2307/2996186

Southwick EE (1984) Photosynthate allocation to floral nectar: a neglected energy investment. Ecology 65:1775-1779. https://doi.org/10.2307/1937773 DOI: https://doi.org/10.2307/1937773

Southwick AK, Southwick EE (1983) Aging effect on nectar production in two clones of Asclepias syriaca. Oecologia 56:121-125. https://doi.org/10.1007/BF00378227 DOI: https://doi.org/10.1007/BF00378227

Strauss SY (1997) Floral characters link herbivores, pollinators, and plant fitness. Ecology 78:1640-1645. https://doi.org/10.1890/0012-9658(1997)078[1640:FCLHPA]2.0.CO;2 DOI: https://doi.org/10.1890/0012-9658(1997)078[1640:FCLHPA]2.0.CO;2

Strauss SY, Whittall JB (2006) Non-pollinator agents of selection on floral traits. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, UK, pp 120-138. https://doi.org/10.1093/oso/9780198570851.003.0007 DOI: https://doi.org/10.1093/oso/9780198570851.003.0007

Thompson KA, Cory KA, Johnson MTJ (2017) Induced defences alter the strength and direction of natural selection on reproductive traits in common milkweed. Journal of Evolutionary Biology 30:1219-1228. https://doi.org/10.1111/jeb.13045 DOI: https://doi.org/10.1111/jeb.13045

Van Zandt PA, Agrawal AA (2004) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616-2629. https://doi.org/10.1890/03-0622 DOI: https://doi.org/10.1890/03-0622

Villalona E, Ezray BD, Laveaga E, Agrawal AA, Ali JG, Hines HM (2020) The role of toxic nectar secondary compounds in driving differential bumble bee preferences for milkweed flowers. Oecologia 193:619-630. https://doi.org/10.1007/s00442-020-04701-0 DOI: https://doi.org/10.1007/s00442-020-04701-0

Willson MF, Bertin RI (1979) Flower-visitors, nectar production, and inflorescence size of Asclepias syriaca. Canadian Journal of Botany 57:1380-1388. https://doi.org/10.1139/b79-172 DOI: https://doi.org/10.1139/b79-172

Willson MF, Rathcke BJ (1974) Adaptive design of the floral display in Asclepias syriaca L. The American Midland Naturalist 92:47-57. https://doi.org/10.2307/2424201 DOI: https://doi.org/10.2307/2424201

Woods EC, Hastings AP, Turley NE, Heard SB, Agrawal AA (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecological Monographs 82:149-168. https://doi.org/10.1890/11-1446.1 DOI: https://doi.org/10.1890/11-1446.1

Wyatt R, Broyles SB, Derda GS (1992) Environmental influences on nectar production in milkweeds (Asclepias syriaca and A. exaltata). American Journal of Botany 79:636-642. https://doi.org/10.1002/j.1537-2197.1992.tb14605.x DOI: https://doi.org/10.1002/j.1537-2197.1992.tb14605.x

Additional Files

Published

2024-03-30

How to Cite

García, Y., Dow, B. ., Vézina, L., & Parachnowitsch, A. (2024). Natural selection by pollinators on floral attractive and defensive traits did not translate into selection via fruits in common milkweed. Journal of Pollination Ecology, 36, 73–84. https://doi.org/10.26786/1920-7603(2024)758

Issue

Section

Articles

Similar Articles

<< < 7 8 9 10 11 12 13 14 15 > >> 

You may also start an advanced similarity search for this article.