Maternal effects in sex-ratio adjustment
Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite Tetranychus urticae
Recommendation: posted 11 June 2018, validated 12 June 2018
Optimal sex ratios have been topic of extensive studies so far. Fisherian 1:1 proportions of males and females are known to be optimal in most (diploid) organisms, but many deviations from this golden rule are observed. These deviations not only attract a lot of attention from evolutionary biologists but also from population ecologists as they eventually determine long-term population growth. Because sex ratios are tightly linked to fitness, they can be under strong selection or plastic in response to changing demographic conditions. Hamilton  pointed out that an equality of the sex ratio breaks down when there is local competition for mates. Competition for mates can be considered as a special case of local resource competition. In short, this theory predicts females to adjust their offspring sex ratio conditional on cues indicating the level of local mate competition that their sons will experience. When cues indicate high levels of LMC mothers should invest more resources in the production of daughters to maximise their fitness, while offspring sex ratios should be closer to 50:50 when cues indicate low levels of LMC.
In isolated populations, Macke et al.  found sex ratio to evolve fast in response to changes in population sex-structure in the spider mite Tetranychus urticae. Spider mites are becoming top-models in evolutionary biology because of their easy housekeeping, fast generation times and well-studied genome . The species is known to respond fast to changes in relatedness and kin-structure by changing its mating strategy , but also dispersal . Sex ratio adjustments are likely mediated by differential investments in egg size, with small eggs possibly experiencing lower chances of fertilization, and thus to develop in haploid males .
Alison Duncan and colleagues  asked the question whether sex ratios change plastically in response to changes in the local population structure. They additionally questioned whether maternal effects could drive changes in sex-allocation of spider mite mothers. Indeed, theory predicts that if environmental changes are predictable across generations, intergenerational plasticity might be more adaptive than intragenerational plasticity . Especially in spatially structured and highly dynamics populations, female spider mites may experience highly variable demographic conditions from one generation to another. During range expansions, spatial variation in local relatedness and inbreeding are documented to change and to impact eco-evolutionary trajectories as well (e.g. ).
Duncan et al.  specifically 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. They surprisingly find the maternal environment to be more important than the actual experienced sex-ratio conditions. These insights thus show the maternal environment to be a reliable predictor of LMC experienced by grand-children. Maternal effects have been found to impact many traits, but this study is the first to convincingly demonstrate maternal effects in sex allocation. It therefore provides an alternative explanation of the apparent fast evolved responses under constant demographic conditions , and adds evidence to the importance of non-genetic trait changes for adaptation towards changing demographic and environmental conditions.
 Hamilton, W. D. (1967). Extraordinary Sex Ratios. Science, 156(3774), 477–488. doi: 10.1126/science.156.3774.477
 Macke, E., Magalhães, S., Bach, F., & Olivieri, I. (2011). Experimental evolution of reduced sex ratio adjustment under local mate competition. Science, 334(6059), 1127–1129. doi: 10.1126/science.1212177
 Grbić, M., Van Leeuwen, T., Clark, R. M., et al. (2011). The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479(7374), 487–492. doi: 10.1038/nature10640
 Macke, E., Magalhães, S., Bach, F., & Olivieri, I. (2012). 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, 279(1747), 4634–4642. doi: 10.1098/rspb.2012.1598
 Bitume, E. V., Bonte, D., Ronce, O., Bach, F., Flaven, E., Olivieri, I., & Nieberding, C. M. (2013). Density and genetic relatedness increase dispersal distance in a subsocial organism. Ecology Letters, 16(4), 430–437. doi: 10.1111/ele.12057
 Duncan, A., Marinosci, C., Devaux, C., Lefèvre, S., Magalhães, S., Griffin, J., Valente, A., Ronce, O., Olivieri, I. (2018). Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite Tetranychus urticae. BioRxiv, 240127, ver. 3. doi: 10.1101/240127
 Petegem, K. V., Moerman, F., Dahirel, M., Fronhofer, E. A., Vandegehuchte, M. L., Leeuwen, T. V., Wybouw, N., Stoks, R., Bonte, D. (2018). Kin competition accelerates experimental range expansion in an arthropod herbivore. Ecology Letters, 21(2), 225–234. doi: 10.1111/ele.12887
 Marshall, D. J., & Uller, T. (2007). When is a maternal effect adaptive? Oikos, 116(12), 1957–1963. doi: 10.1111/j.2007.0030-1299.16203.x
Dries Bonte (2018) Maternal effects in sex-ratio adjustment. Peer Community in Evolutionary Biology, 100051. 10.24072/pci.evolbiol.100051
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.
Evaluation round #2
DOI or URL of the preprint: 10.1101/240127
Version of the preprint: 2
Author's Reply, 07 Jun 2018
Decision by Dries Bonte, posted 07 Jun 2018
I obtained comments from one reviewer and read the manuscript carefully as well. As you will see, we are nearly there - this make a nice contribution to the literature on putative adaptive maternal effects.
While the reviewer comes up with some textual edits, i read it through the glasses of a non-expert audience (so to make it digestible for a wider audience) and have a few comments:
line 24: within the local, rather than isolated
lines 47-49: can you add a sentence on the reasoning, as this is an additional mechanisms not explained earlier
line 80: add 'the parasitoid wasp’
lines 303-305: needs a couple of sentences to explain
lines 394-395: but they are likely present if they recognise kin(d). From an adaptive perspective the cues from mothers should then be more reliable than those obtained directly, or allow a much faster response to avoid LMC (no lags)
Looking forward to finalise this procedure!
Reviewed by anonymous reviewer, 15 Apr 2018
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/240127
Version of the preprint: 1
Author's Reply, 11 Apr 2018
Decision by Dries Bonte, posted 11 Apr 2018
Alison Duncan and colleagues investigated their role of maternal effects and sib mating on offspring sex-ratios. They conducted several laboratory experiments in which maternal LMC was manipulated by changing the number of founders, while maintaining density. The paper is to my opinion well written, data well analysed and collected.
The reviewers agree with my evaluation but came up with several issues that the authors want to take into account to improve their paper. While I found the reasoning regarding predictability well explained (I am also of opinion that the perspective of local information not matching cross-generationally integrated population-level information is indeed key to understand many demographic dynamics), the reviewers want to see some aspects of the reasoning better worked out. Reviewer one questions the validity of the experiments because of putative problems with the experimental setup and the used patch sizes. As a recommender of your manuscript, I believe issues on this can be avoided by providing a schematic presentation of your breeding design. Especially the descriptions on the different sample sizes (patches) in the quarters of the boxes are hard (not to say impossible) to understand since no reasoning for this setup is given. I recommend the authors to make this part clearer to the audience, as this information seems central to understand the potential drivers of the recorded maternal effects on offspring sex ratio.
In addition, the authors should provide the raw data (e.g. in supplementary material) or the link to the raw data if they are deposited on an open repository. Similarly, the authors should give more details about their statistical analysis (a SAS script would be particularly welcome). These requirements are indicated in the PCI ethical code of conduct (https://evolbiol.peercommunityin.org/about/ethics).