Section: Evolutionary Biology
Topic: Evolution, Population biology

Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations

Deere, Jacques A.1  ; Smallegange, Isabel M.2   
1 Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, PO Box 94240, 1090 GE Amsterdam, the Netherlands
2 School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK

10.24072/pcjournal.351 - Peer Community Journal, Volume 3 (2023), article no. e117.

Get full text PDF Peer reviewed and recommended by PCI
article image

Developmental plasticity alters phenotypes and can in that way change the response to selection. When alternative phenotypes show different life history trajectories, developmental plasticity can also affect, and be affected by, population size-structure in an eco-evolutionary interaction. Developmental plasticity often functions to anticipate future conditions but it can also mitigate current stress conditions. Both types of developmental plasticity have evolved under different selections and this raises the question if they underlie different eco-evolutionary population dynamics. Here, we tested, in a long-term population experiment using the male polyphenic bulb mite (Rhizoglyphus robini), if the selective harvesting of juveniles of different developmental stages concurrently alters population size (ecological response) and male adult phenotype expression (evolutionary response) in line with eco-evolutionary predictions that assume the male polyphenism is anticipatory or mitigating. We found that the frequency of adult males that expressed costly (fighter) morphology was lowest under the most severe juvenile harvesting conditions. This response cannot be explained if we assume that adult male phenotype expression is to anticipate adult (mating) conditions because, in that case, only the manipulation of adult performance would have an effect. Instead, we suggest that juveniles mitigate their increased mortality risk by expediating ontogeny to forego the development of costly morphology and mature quicker but as a defenceless scrambler. If, like in mammals and birds where early-life stress effects are extensively studied, we account for such pre-adult viability selection in coldblooded species, it would allow us to (i) better characterise natural selection on trait development like male polyphenisms, (ii) understand how it can affect the response to other selections in adulthood, and (iii) understand how such trait dynamics influence, and are influenced by, population dynamics.

Published online:
DOI: 10.24072/pcjournal.351
Type: Research article
Keywords: alternative male phenotypes, dispersal, eco-evolutionary dynamics, male morph coexistence, polyphenism

Deere, Jacques A. 1; Smallegange, Isabel M. 2

1 Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, PO Box 94240, 1090 GE Amsterdam, the Netherlands
2 School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_351,
     author = {Deere, Jacques A. and Smallegange, Isabel M.},
     title = {Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations},
     journal = {Peer Community Journal},
     eid = {e117},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.351},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.351/}
}
TY  - JOUR
AU  - Deere, Jacques A.
AU  - Smallegange, Isabel M.
TI  - Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.351/
DO  - 10.24072/pcjournal.351
LA  - en
ID  - 10_24072_pcjournal_351
ER  - 
%0 Journal Article
%A Deere, Jacques A.
%A Smallegange, Isabel M.
%T Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.351/
%R 10.24072/pcjournal.351
%G en
%F 10_24072_pcjournal_351
Deere, Jacques A.; Smallegange, Isabel M. Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations. Peer Community Journal, Volume 3 (2023), article  no. e117. doi : 10.24072/pcjournal.351. https://peercommunityjournal.org/articles/10.24072/pcjournal.351/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100647

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Badyaev, A. V. Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation, Proceedings of the Royal Society B: Biological Sciences, Volume 272 (2005) no. 1566, pp. 877-886 | DOI

[2] Buzatto, B. A.; Machado, G. Male dimorphism and alternative reproductive tactics in harvestmen (Arachnida: Opiliones), Behavioural Processes, Volume 109 (2014), pp. 2-13 | DOI

[3] Carr, A. L.; Roe, M. Acarine attractants: Chemoreception, bioassay, chemistry and control, Pesticide Biochemistry and Physiology, Volume 131 (2016), pp. 60-79 | DOI

[4] Casasa, S.; Zattara, E. E.; Moczek, A. P. Nutrition-responsive gene expression and the developmental evolution of insect polyphenism, Nature Ecology & Evolution, Volume 4 (2020) no. 7, pp. 970-978 | DOI

[5] Cotton, S.; Fowler, K.; Pomiankowski, A. Condition dependence of sexual ornament size and variation in the stalk-eyed fly Cyrtodiopsis dalmanni (diptera: diopsidae), Evolution, Volume 58 (2004) no. 5, pp. 1038-1046 | DOI

[6] Dawkins, R. Good Strategy or Evolutionarily Stable Strategy?, Sociobiology: Beyond Nature/Nurture?, Routledge, 2019, pp. 331-367 | DOI

[7] Deere, J. A.; Coulson, T.; Smallegange, I. M. Life History Consequences of the Facultative Expression of a Dispersal Life Stage in the Phoretic Bulb Mite (Rhizoglyphus robini), PLOS ONE, Volume 10 (2015) no. 9 | DOI

[8] Deere, J. A.; Smallegange, I. M. Does frequency-dependence determine male morph survival in the bulb mite Rhizoglyphus robini?, Experimental and Applied Acarology, Volume 62 (2013) no. 4, pp. 425-436 | DOI

[9] Deere, J.; Smallegange, I. Data and analysis of "Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations, figshare, 2023 | DOI

[10] Del Giudice, M.; Buck, C. L.; Chaby, L. E.; Gormally, B. M.; Taff, C. C.; Thawley, C. J.; Vitousek, M. N.; Wada, H. What Is Stress? A Systems Perspective, Integrative and Comparative Biology, Volume 58 (2018) | DOI

[11] Díaz, A.; Okabe, K.; Eckenrode, C.; Villani, M.; Oconnor, B. Biology, ecology, and management of the bulb mites of the genus Rhizoglyphus (Acari: Acaridae), Experimental and Applied Acarology, Volume 24 (2000) no. 2, pp. 85-113 | DOI

[12] Eberhard, W. G. Beetle Horn Dimorphism: Making the Best of a Bad Lot, The American Naturalist, Volume 119 (1982) no. 3, pp. 420-426 | DOI

[13] Edeline, E.; Loeuille, N. Size‐dependent eco‐evolutionary feedbacks in harvested systems, Oikos, Volume 130 (2021) no. 10, pp. 1636-1649 | DOI

[14] Ellis, B. J.; Del Giudice, M. Developmental Adaptation to Stress: An Evolutionary Perspective, Annual Review of Psychology, Volume 70 (2019) no. 1, pp. 111-139 | DOI

[15] Ernande, B.; Dieckmann, U.; Heino, M. Adaptive changes in harvested populations: plasticity and evolution of age and size at maturation, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 271 (2004) no. 1537, pp. 415-423 | DOI

[16] Fisher, M. O.; Nager, R. G.; Monaghan, P. Compensatory Growth Impairs Adult Cognitive Performance, PLoS Biology, Volume 4 (2006) no. 8 | DOI

[17] Forsman, A. Rethinking phenotypic plasticity and its consequences for individuals, populations and species, Heredity, Volume 115 (2014) no. 4, pp. 276-284 | DOI

[18] Gardner, J. L.; Peters, A.; Kearney, M. R.; Joseph, L.; Heinsohn, R. Declining body size: a third universal response to warming?, Trends in Ecology & Evolution, Volume 26 (2011) no. 6, pp. 285-291 | DOI

[19] Gibert, J. P.; Han, Z.; Wieczynski, D. J.; Votzke, S.; Yammine, A. Feedbacks between size and density determine rapid eco‐phenotypic dynamics, Functional Ecology, Volume 36 (2022) no. 7, pp. 1668-1680 | DOI

[20] Griffiths, P. E.; Gray, R. D. Developmental Systems and Evolutionary Explanation, Journal of Philosophy, Volume 91 (1994) no. 6, pp. 277-304 | DOI

[21] Hazel, W.; Smock, R.; Johnson, M. A polygenic model for the evolution and maintenance of conditional strategies, Proceedings of the Royal Society of London. Series B: Biological Sciences, Volume 242 (1990) no. 1305, pp. 181-187 | DOI

[22] Hazel, W.; Smock, R.; Lively, C. M. The Ecological Genetics of Conditional Strategies, The American Naturalist, Volume 163 (2004) no. 6, pp. 888-900 | DOI

[23] Hill, G. E. Condition-dependent traits as signals of the functionality of vital cellular processes, Ecology Letters, Volume 14 (2011) no. 7, pp. 625-634 | DOI

[24] Hilborn, R.; Walters, C. J. Quantitative Fisheries Stock Assessment, Springer US, Boston, MA, 1992 | DOI

[25] Huryn, A. D.; Benke, A. C. Relationship between biomass turnover and body size for stream communities, Body Size: The Structure and Function of Aquatic Ecosystems, Cambridge University Press, 2007, pp. 55-76 | DOI

[26] Knell, R. J.; Martínez-Ruiz, C. Selective harvest focused on sexual signal traits can lead to extinction under directional environmental change, Proceedings of the Royal Society B: Biological Sciences, Volume 284 (2017) no. 1868 | DOI

[27] Lindström, J. Early development and fitness in birds and mammals, Trends in Ecology & Evolution, Volume 14 (1999) no. 9, pp. 343-348 | DOI

[28] Lürig, M. D.; Matthews, B. Dietary-based developmental plasticity affects juvenile survival in an aquatic detritivore, Proceedings of the Royal Society B: Biological Sciences, Volume 288 (2021) no. 1945 | DOI

[29] Moczek, A. P. The behavioral ecology of threshold evolution in a polyphenic beetle, Behavioral Ecology, Volume 14 (2003) no. 6, pp. 841-854 | DOI

[30] Mojica, J. P.; Kelly, J. K. Viability selection prior to trait expression is an essential component of natural selection, Proceedings of the Royal Society B: Biological Sciences, Volume 277 (2010) no. 1696, pp. 2945-2950 | DOI

[31] Nijhout, H. F.; McKenna, K. Z. The distinct roles of insulin signaling in polyphenic development, Current Opinion in Insect Science, Volume 25 (2018), pp. 58-64 | DOI

[32] Plaistow, S. J.; Tsuchida, K.; Tsubaki, Y.; Setsuda, K. The effect of a seasonal time constraint on development time, body size, condition, and morph determination in the horned beetle Allomyrina dichotoma L. (Coleoptera: Scarabaeidae), Ecological Entomology, Volume 30 (2005) no. 6, pp. 692-699 | DOI

[33] Radwan, J. Male morph determination in two species of acarid mites, Heredity, Volume 74 (1995) no. 6, pp. 669-673 | DOI

[34] Radwan, J.; Bogacz, I. Comparison of life-history traits of the two male morphs of the bulb mite, Rhizoglyphus robini, Experimental and Applied Acarology, Volume 24 (2000) no. 2, pp. 115-121 | DOI

[35] Radwan, J.; Czyż, M.; Konior, M.; Kolodziejczyk, M. Aggressiveness in Two Male Morphs of the Bulb Mite Rhizoglyphus robini, Ethology, Volume 106 (2000) no. 1, pp. 53-62 | DOI

[36] Rhebergen, F. The ecology of adaptive condition-dependent polyphenism, PhD thesis, University of Amsterdam, The Netherlands (2022)

[37] Rhebergen, F. T.; Stewart, K. A.; Smallegange, I. M. Nutrient-dependent allometric plasticity in a male-diphenic mite, Ecology and Evolution, 2022 | DOI

[38] Roff, D. A. The Evolution of Threshold Traits in Animals, The Quarterly Review of Biology, Volume 71 (1996) no. 1, pp. 3-35 | DOI

[39] Sasson, D. A.; Munoz, P. R.; Gezan, S. A.; Miller, C. W. Resource quality affects weapon and testis size and the ability of these traits to respond to selection in the leaf‐footed cactus bug, Narnia femorata, Ecology and Evolution, Volume 6 (2016) no. 7, pp. 2098-2108 | DOI

[40] Schaefer, M. Some aspects of the dynamics of populations important to the management of commercial marine fisheries. , Inter-Americal Tropical Tuna Commission Bulletin, Volume 1, 1954, pp. 23-56

[41] Sheridan, J. A.; Bickford, D. Shrinking body size as an ecological response to climate change, Nature Climate Change, Volume 1 (2011) no. 8, pp. 401-406 | DOI

[42] Shuster, S. M.; Wade, M. J. Mating Systems and Strategies, Princeton University Press, 2003 | DOI

[43] Smallegange, I. M. Complex environmental effects on the expression of alternative reproductive phenotypes in the bulb mite, Evolutionary Ecology, Volume 25 (2010) no. 4, pp. 857-873 | DOI

[44] Smallegange, I. M. Integrating developmental plasticity into eco-evolutionary population dynamics, Trends in Ecology & Evolution, Volume 37 (2022) no. 2, pp. 129-137 | DOI

[45] Smallegange, I. M.; Coulson, T. The stochastic demography of two coexisting male morphs, Ecology, Volume 92 (2011) no. 3, pp. 755-764 | DOI

[46] Smallegange, I. M.; Coulson, T. Towards a general, population-level understanding of eco-evolutionary change, Trends in Ecology & Evolution, Volume 28 (2013) no. 3, pp. 143-148 | DOI

[47] Smallegange, I. M.; Deere, J. A. Eco-Evolutionary Interactions as a Consequence of Selection on a Secondary Sexual Trait, Eco-Evolutionary Dynamics, Elsevier, 2014, pp. 145-169 | DOI

[48] Smallegange, I. M.; Ens, H. M. Trait‐based predictions and responses from laboratory mite populations to harvesting in stochastic environments, Journal of Animal Ecology, Volume 87 (2018) no. 4, pp. 893-905 | DOI

[49] Smallegange, I. M.; Rhebergen, F. T.; Stewart, K. A. Cross-level considerations for explaining selection pressures and the maintenance of genetic variation in condition-dependent male morphs, Current Opinion in Insect Science, Volume 36 (2019), pp. 66-73 | DOI

[50] Steiner, U. K. What determines whether to scramble or fight in male bulb mites, Peer Community in Evolutionary Biology (2023) | DOI

[51] Stewart, K. A.; Draaijer, R.; Kolasa, M. R.; Smallegange, I. M. The role of genetic diversity in the evolution and maintenance of environmentally-cued, male alternative reproductive tactics, BMC Evolutionary Biology, Volume 19 (2019) no. 1 | DOI

[52] Tomkins, J. L.; Hazel, W. N.; Penrose, M. A.; Radwan, J. W.; LeBas, N. R. Habitat Complexity Drives Experimental Evolution of a Conditionally Expressed Secondary Sexual Trait, Current Biology, Volume 21 (2011) no. 7, pp. 569-573 | DOI

[53] Travis, J.; Leips, J.; Rodd, F. H. Evolution in Population Parameters: Density-Dependent Selection or Density-Dependent Fitness?, The American Naturalist, Volume 181 (2013) no. S1 | DOI

[54] Van den Beuken, T. P. G.; Duinmeijer, C. C.; Smallegange, I. M. Costs of weaponry: Unarmed males sire more offspring than armed males in a male‐dimorphic mite, Journal of Evolutionary Biology, Volume 32 (2018) no. 2, pp. 153-162 | DOI

[55] van Gils, J. A.; Lisovski, S.; Lok, T.; Meissner, W.; Ożarowska, A.; de Fouw, J.; Rakhimberdiev, E.; Soloviev, M. Y.; Piersma, T.; Klaassen, M. Body shrinkage due to Arctic warming reduces red knot fitness in tropical wintering range, Science, Volume 352 (2016) no. 6287, pp. 819-821 | DOI

[56] Verhulst, P. Notice sur la loi que la population suit dans son accroissement, Correspondance Mathématique et Physique, Volume 10 (1838), pp. 113-121

[57] Vickers, M. Early Life Nutrition, Epigenetics and Programming of Later Life Disease, Nutrients, Volume 6 (2014) no. 6, pp. 2165-2178 | DOI

[58] Weir, L. K.; Kindsvater, H. K.; Young, K. A.; Reynolds, J. D. Sneaker Males Affect Fighter Male Body Size and Sexual Size Dimorphism in Salmon, The American Naturalist, Volume 188 (2016) no. 2, pp. 264-271 | DOI

[59] Wells, J. C. The thrifty phenotype: An adaptation in growth or metabolism?, American Journal of Human Biology, Volume 23 (2010) no. 1, pp. 65-75 | DOI

[60] West-Eberhard, M. J. Developmental Plasticity and Evolution, Oxford University Press, 2003 | DOI

Cited by Sources: