Section: Evolutionary Biology
Topic: Evolution, Population biology

Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite Tetranychus urticae

10.24072/pcjournal.343 - Peer Community Journal, Volume 3 (2023), article no. e108.

Get full text PDF Peer reviewed and recommended by PCI

In structured populations, competition for mates between closely related males, termed Local Mate Competition (LMC), is expected to select for female-biased offspring sex ratios. However, the cues underlying sex allocation decisions remain poorly studied. Here, we test for several cues in the spider mite Tetranychus urticae, a species that was previously found to adjust the sex ratio of its offspring in response to the number of females within the local population, i.e. a patch. We here investigate whether the offspring sex ratio of T. urticae females changes in response to 1) the current number of females in the same patch, 2) the number of females in the patches of their mothers and 3) their relatedness to their mate. Single females on patches produced similar sex ratios to those of groups of 15 females; their mothers had been in identical conditions of panmixia. The offspring sex ratios of females mated with their brother did not differ from those of females mated with an unrelated male. Females however produced a more female-biased offspring sex ratio if their mothers were alone on a patch compared to 15 other females. Thus, maternal environment is used as a cue for the sex allocation of daughters. We discuss the conditions under which the maternal environment may be a reliable predictor of LMC experienced by grand-sons.

Published online:
DOI: 10.24072/pcjournal.343
Type: Research article
Keywords: local mate competition, sex-ratio, sib-mating, haplodiploid
Duncan, Alison B. 1; Marinosci, Cassandra 1; Devaux, Céline 1; Lefèvre, Sophie 1; Magalhães, Sara 2; Griffin, Joanne 1; Valente, Adeline 1; Ronce, Ophélie 1; Olivieri, Isabelle 1

1 ISEM, Université de Montpellier, CNRS, IRD, EPHE, CC065, Place Eugène Bataillon, 34095 Montpellier Cedex 05, France
2 cE3c: Centre for Ecology, Evolution, and Environmental Changes, Faculty of Sciences, University of Lisbon, Edifício C2, 38 piso, 1749-016 Lisboa, Portugal
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
@article{10_24072_pcjournal_343,
     author = {Duncan, Alison B. and Marinosci, Cassandra and Devaux, C\'eline and Lef\`evre, Sophie and Magalh\~aes, Sara and Griffin, Joanne and Valente, Adeline and Ronce, Oph\'elie and Olivieri, Isabelle},
     title = {Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite {\protect\emph{Tetranychus} urticae}},
     journal = {Peer Community Journal},
     eid = {e108},
     publisher = {Peer Community In},
     volume = {3},
     year = {2023},
     doi = {10.24072/pcjournal.343},
     language = {en},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.343/}
}
TY  - JOUR
AU  - Duncan, Alison B.
AU  - Marinosci, Cassandra
AU  - Devaux, Céline
AU  - Lefèvre, Sophie
AU  - Magalhães, Sara
AU  - Griffin, Joanne
AU  - Valente, Adeline
AU  - Ronce, Ophélie
AU  - Olivieri, Isabelle
TI  - Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite Tetranychus urticae
JO  - Peer Community Journal
PY  - 2023
VL  - 3
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.343/
DO  - 10.24072/pcjournal.343
LA  - en
ID  - 10_24072_pcjournal_343
ER  - 
%0 Journal Article
%A Duncan, Alison B.
%A Marinosci, Cassandra
%A Devaux, Céline
%A Lefèvre, Sophie
%A Magalhães, Sara
%A Griffin, Joanne
%A Valente, Adeline
%A Ronce, Ophélie
%A Olivieri, Isabelle
%T Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite Tetranychus urticae
%J Peer Community Journal
%D 2023
%V 3
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.343/
%R 10.24072/pcjournal.343
%G en
%F 10_24072_pcjournal_343
Duncan, Alison B.; Marinosci, Cassandra; Devaux, Céline; Lefèvre, Sophie; Magalhães, Sara; Griffin, Joanne; Valente, Adeline; Ronce, Ophélie; Olivieri, Isabelle. Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite Tetranychus urticae. Peer Community Journal, Volume 3 (2023), article  no. e108. doi : 10.24072/pcjournal.343. https://peercommunityjournal.org/articles/10.24072/pcjournal.343/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100051

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] Abe, J.; Kamimura, Y.; West, S. A. Inexplicably Female-Biased Sex Ratios In Melittobia Wasps, Evolution, Volume 68 (2014) no. 9, pp. 2709-2717 | DOI

[2] Barks, P. M.; Laird, R. A. Senescence in duckweed: age‐related declines in survival, reproduction and offspring quality, Functional Ecology, Volume 29 (2014) no. 4, pp. 540-548 | DOI

[3] Bentz, A. B.; Becker, D. J.; Navara, K. J. Evolutionary implications of interspecific variation in a maternal effect: a meta-analysis of yolk testosterone response to competition, Royal Society Open Science, Volume 3 (2016) no. 11 | DOI

[4] Bitume, E. V.; Bonte, D.; Ronce, O.; Bach, F.; Flaven, E.; Olivieri, I.; Nieberding, C. M. Density and genetic relatedness increase dispersal distance in a subsocial organism, Ecology Letters, Volume 16 (2013) no. 4, pp. 430-437 | DOI

[5] Bitume, E. V.; Bonte, D.; Ronce, O.; Olivieri, I.; Nieberding, C. M. Dispersal distance is influenced by parental and grand-parental density, Proceedings of the Royal Society B: Biological Sciences, Volume 281 (2014) no. 1790 | DOI

[6] Bonte, D. Maternal Effects in Sex-Ratio Adjustment, Peer Community in Evolutionary Biology, Volume 100051 (2018) | DOI

[7] Bowers, E. K.; Thompson, C. F.; Sakaluk, S. K. Maternal Natal Environment and Breeding Territory Predict the Condition and Sex Ratio of Offspring, Evolutionary Biology, Volume 44 (2016) no. 1, pp. 11-20 | DOI

[8] Burton‐Chellew, M. N.; Koevoets, T.; Grillenberger, B. K.; Sykes, E. M.; Underwood, S. L.; Bijlsma, K.; Gadau, J.; Zande, L. v. d.; Beukeboom, L. W.; West, S. A.; Shuker, D. M. Facultative Sex Ratio Adjustment in Natural Populations of Wasps: Cues of Local Mate Competition and the Precision of Adaptation, The American Naturalist, Volume 172 (2008) no. 3, pp. 393-404 | DOI

[9] Charnov, E. The Theory of Sex Allocation, Princeton University Press, 1982

[10] Clotuche, G.; Yano, S.; Akino, T.; Amano, H. Chemical investigation of aggregation behaviour in the two-spotted spider mite Tetranychus urticae, Experimental and Applied Acarology, Volume 63 (2014) no. 3, pp. 377-387 | DOI

[11] Duncan, A. B.; Marinosci, C.; Devaux, C.; Lefèvre, S.; Magalhães, S.; Griffin, J.; Valente, A.; Ronce, O.; Olivieri, I. Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite Tetranychus urticae, bioRxiv, 2018 | DOI

[12] Edwards, A. M.; Cameron, E. Z.; Pereira, J. C.; Wapstra, E.; Ferguson-Smith, M. A.; Horton, S. R.; Thomasson, K. Gestational experience alters sex allocation in the subsequent generation, Royal Society Open Science, Volume 3 (2016) no. 7 | DOI

[13] Feiertag-Koppen, C.; Pijnacker, L. Development of the female germ cells and process of internal fertilization in the two-spotted spider mite Tetranychus urticae koch (Acariformes : Tetranychidae), International Journal of Insect Morphology and Embryology, Volume 11 (1982) no. 5-6, pp. 271-284 | DOI

[14] Frank, S. A. Hierarchical Selection Theory And Sex Ratios. II. On Applying The Theory, And A Test With Fig Wasps, Evolution, Volume 39 (1985) no. 5, pp. 949-964 | DOI

[15] Gardner, A.; Arce, A.; Alpedrinha, J. Budding dispersal and the sex ratio, Journal of Evolutionary Biology, Volume 22 (2009) no. 5, pp. 1036-1045 | DOI

[16] Greeff, J. M. Alternative mating strategies, partial sibmating and split sex ratios in haplodiploid species, Journal of Evolutionary Biology, Volume 9 (1996) no. 6, pp. 855-869 | DOI

[17] Hamilton, W. D. Extraordinary Sex Ratios, Science, Volume 156 (1967) no. 3774, pp. 477-488 | DOI

[18] Helle, H.; Koskela, E.; Mappes, T. Life in varying environments: experimental evidence for delayed effects of juvenile environment on adult life history, Journal of Animal Ecology, Volume 81 (2011) no. 3, pp. 573-582 | DOI

[19] Helle, M.; Sabelis, M. Spider mites: Their biology, natural enemies and control, World Crop Pests, 1, Elsevier, Amsterdam-New York, 1985

[20] Herre, E. A. Sex Ratio Adjustment in Fig Wasps, Science, Volume 228 (1985) no. 4701, pp. 896-898 | DOI

[21] Innocent, T. M.; Savage, J.; West, S. A.; Reece, S. E. Lethal combat and sex ratio evolution in a parasitoid wasp, Behavioral Ecology, Volume 18 (2007) no. 4, pp. 709-715 | DOI

[22] Lievens, E. J.; Henriques, G. J.; Michalakis, Y.; Lenormand, T. Maladaptive Sex Ratio Adjustment in the Invasive Brine Shrimp Artemia franciscana, Current Biology, Volume 26 (2016) no. 11, pp. 1463-1467 | DOI

[23] Little, T. J.; O'Connor, B.; Colegrave, N.; Watt, K.; Read, A. F. Maternal Transfer of Strain-Specific Immunity in an Invertebrate, Current Biology, Volume 13 (2003) no. 6, pp. 489-492 | DOI

[24] Macke, E.; Magalhães, S.; Bach, F.; Olivieri, I. Experimental Evolution of Reduced Sex Ratio Adjustment Under Local Mate Competition, Science, Volume 334 (2011) no. 6059, pp. 1127-1129 | DOI

[25] Macke, E.; Magalhães, S.; Bach, F.; Olivieri, I. Sex-ratio adjustment in response to local mate competition is achieved through an alteration of egg size in a haplodiploid spider mite, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2012) no. 1747, pp. 4634-4642 | DOI

[26] Macke, E.; Magalhães, S.; Khan, H. D.-T.; Luciano, A.; Frantz, A.; Facon, B.; Olivieri, I. Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch, Proceedings of the Royal Society B: Biological Sciences, Volume 278 (2010) no. 1708, pp. 1054-1063 | DOI

[27] Macke, E.; Olivieri, I.; Magalhães, S. Local Mate Competition Mediates Sexual Conflict over Sex Ratio in a Haplodiploid Spider Mite, Current Biology, Volume 24 (2014) no. 23, pp. 2850-2854 | DOI

[28] Magalhães, S.; Fayard, J.; Janssen, A.; Carbonell, D.; Olivieri, I. Adaptation in a spider mite population after long‐term evolution on a single host plant, Journal of Evolutionary Biology, Volume 20 (2007) no. 5, pp. 2016-2027 | DOI

[29] Magalhães, S.; Blanchet, E.; Egas, M.; Olivieri, I. Environmental effects on the detection of adaptation, Journal of Evolutionary Biology, Volume 24 (2011) no. 12, pp. 2653-2662 | DOI

[30] Marinosci, C.; Magalhães, S.; Macke, E.; Navajas, M.; Carbonell, D.; Devaux, C.; Olivieri, I. Effects of host plant on life‐history traits in the polyphagous spider mite Tetranychus urticae, Ecology and Evolution, Volume 5 (2015) no. 15, pp. 3151-3158 | DOI

[31] Maynard Smith, J. The Evolution of Sex, Cambridge University Press, Cambridge, 1978

[32] Migeon, A.; Dorkeld, F. Spider Mites Web: A Comprehensive Database for the Tetranychidae, 2006 (https://www1.montpellier.inra.fr/CBGP/spmweb)

[33] Mothes-Wagner, U. Post-embryonic development of the two-spotted spider mite Tetranychus urticae with special reference to the differentiation of the female reproductive system, International Journal of Invertebrate Reproduction and Development, Volume 7 (1984) no. 4, pp. 203-216 | DOI

[34] Mousseau, T. The adaptive significance of maternal effects, Trends in Ecology & Evolution, Volume 13 (1998) no. 10, pp. 403-407 | DOI

[35] Nagelkerke, C. J.; Sabelis, M. W. Hierarchical Levels of Spatial Structure and Their Consequences for the Evolution of Sex Allocation in Mites and Other Arthropods, The American Naturalist, Volume 148 (1996) no. 1, pp. 16-39 | DOI

[36] Oku, K.; Yano, S.; Takafuji, A. Different maternal effects on diapause induction of tetranychid mites, Tetranychus urticae and T. kanzawai (Acari: Tetranychidae), Applied Entomology and Zoology, Volume 38 (2003) no. 2, pp. 267-270 | DOI

[37] Pallini, A.; Janssen, A.; Sabelis, M. Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors, Oecologia, Volume 110 (1997), pp. 179-185 | DOI

[38] Pick, J. L.; Ebneter, C.; Hutter, P.; Tschirren, B. Disentangling Genetic and Prenatal Maternal Effects on Offspring Size and Survival, The American Naturalist, Volume 188 (2016) no. 6, pp. 628-639 | DOI

[39] Reece, S. E.; Shuker, D. M.; Pen, I.; Duncan, A. B.; Choudhary, A.; Batchelor, C. M.; West, S. A. Kin discrimination and sex ratios in a parasitoid wasp, Journal of Evolutionary Biology, Volume 17 (2003) no. 1, pp. 208-216 | DOI

[40] Reece, S.; Wherry, R.; Bloor, J. Sex Allocation and Interactions between Relatives in the Bean Beetle, Callosobruchus Maculatus, Behav. Processes, Volume 70 (2005), pp. 282-288 | DOI

[41] Riahi, E.; Shishehbor, P.; Nemati, A.; Saeidi, Z. Temperature effects on development and life table parameters of Tetranychus urticae (Acari: Tetranychidae, Volume 15 (2013), pp. 661-672 (http://dorl.net/dor/20.1001.1.16807073.2013.15.4.15.8)

[42] Roeder, C. M. Sex ratio response of the two-spotted spider mite (Tetranychus urticae Koch) to changes in density under local mate competition, Canadian Journal of Zoology, Volume 70 (1992) no. 10, pp. 1965-1967 | DOI

[43] Royalty, R. N.; Phelan, P. L.; Hall, F. R. Arrestment of male twospotted spider mite caused by female sex pheromone, Journal of Chemical Ecology, Volume 18 (1992) no. 2, pp. 137-153 | DOI

[44] Sato, Y.; Saito, Y. Can the extremely female‐biased sex ratio of the social spider mites be explained by Hamilton’s local mate competition model?, Ecological Entomology, Volume 32 (2007) no. 6, pp. 597-602 | DOI

[45] Sheriff, M. J.; Love, O. P. Determining the adaptive potential of maternal stress, Ecology Letters, Volume 16 (2012) no. 2, pp. 271-280 | DOI

[46] Shuker, D. M.; Cook, N. Evolution: Conflict by the Sexes, for the Sexes, Current Biology, Volume 24 (2014) no. 23 | DOI

[47] Shuker, D. M.; Moynihan, A. M.; Ross, L. Sexual conflict, sex allocation and the genetic system, Biology Letters, Volume 5 (2009) no. 5, pp. 682-685 | DOI

[48] Shuker, D. M.; Pen, I.; Duncan, A. B.; Reece, S. E.; West, S. A. Sex Ratios under Asymmetrical Local Mate Competition: Theory and a Test with Parasitoid Wasps, The American Naturalist, Volume 166 (2005) no. 3, pp. 301-316 | DOI

[49] Shuker, D. M.; Reece, S. E.; Lee, A.; Graham, A.; Duncan, A. B.; West, S. A. Information use in space and time: sex allocation behaviour in the parasitoid wasp Nasonia vitripennis, Animal Behaviour, Volume 73 (2007) no. 6, pp. 971-977 | DOI

[50] Shuker, D. M.; West, S. A. Information constraints and the precision of adaptation: Sex ratio manipulation in wasps, Proceedings of the National Academy of Sciences, Volume 101 (2004) no. 28, pp. 10363-10367 | DOI

[51] Taylor, P. Intra-Sex and Inter-Sex Sibling Interactions, Nature, Volume 291 (1981), pp. 64-66 | DOI

[52] Tien, N. S. H.; Massourakis, G.; Sabelis, M. W.; Egas, M. Mate choice promotes inbreeding avoidance in the two-spotted spider mite, Experimental and Applied Acarology, Volume 54 (2011) no. 2, pp. 119-124 | DOI

[53] Tien, N.; Sabelis, M.; Egas, M. Inbreeding Depression and Purging in a Haplodiploid: Gender-Related Effects, Heredity, Volume 114 (2014), pp. 327-332 | DOI

[54] Wang, R.-W.; Sun, B.-F.; He, J.-Z.; Dunn, D. W. Non-quantitative adjustment of offspring sex ratios in pollinating fig wasps, Scientific Reports, Volume 5 (2015) no. 1 | DOI

[55] Warner, D. A.; Uller, T.; Shine, R. Transgenerational sex determination: the embryonic environment experienced by a male affects offspring sex ratio, Scientific Reports, Volume 3 (2013) no. 1 | DOI

[56] West, S. A.; Shuker, D. M.; Sheldon, B. C. Sex-ratio adjustment when relatives interact: a test of constraints on adaptation, Evolution, Volume 59 (2005) no. 6, pp. 1211-1228 | DOI

[57] Wrensch, D. L.; Young, S. Effects of Density and Host Quality on Rate of Development, Survivorship, and Sex Ratio in the Carmine Spider Mite 1, Environmental Entomology, Volume 7 (1978) no. 4, pp. 499-501 | DOI

[58] Yoshioka, T.; Yano, S. Do Tetranychus urticae males avoid mating with familiar females?, Journal of Experimental Biology (2014) | DOI

Cited by Sources: