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14 Jan 2021
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Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case study

Tell us how you can be, and we’ll make you better: exploiting genetic variability in personality traits to improve top-down control of agricultural pests

Recommended by based on reviews by Bart A Pannebakker, François Dumont, Joshua Patrick Byrne and Ana Pimenta Goncalves Pereira

Agriculture in the XXI century faces the huge challenge of having to provide food to a rapidly growing human population, which is expected to reach 10.9 billion in 2100 (UUNN 2019), by means of practices and methods that guarantee crop sustainability, human health safety, and respect to the environment (UUNN 2015). Such regulation by the United Nations ultimately entails that agricultural scientists are urged to design strategies and methods that effectively minimize the use of harmful chemical products to control pest populations and to improve soil quality.
One of the most, if not the most, sustainable, safe, and environmentally friendly approach to apply against pests is Biological Pest Control (BPC, hereafter), that is, the use of natural enemies to control the populations of pest organisms. The concept of BPC is by no means new: long back to the 300 AC, Chinese farmers built bamboo bridges between citrus trees to facilitate the foraging of the ant species Oecophylla smaragdina to control lepidopteran citrus pests (Konishi and Ito, 1973); It is also nice to use this recommendation letter to recall and quote the words written in 1752 by the famous Swedish taxonomist, botanist and zoologist, Carl Linnaeus: "Every insect has its predator which follows and destroys it. Such predatory insects should be caught and used for disinfecting crop-plants" (Hörstadius (1974) apud Linnaeus 1752).
Acknowledging the many cases of successes from BPC along our recent history, it is also true that application of BPC strategies during the XX century suffered from wrong-doings, mainly when the introduced biological control agent (BCA, hereafter) was of exotic origin and with a generalist diet-breath; in some cases the release of exotic species resulted on global extinction, reduction in the range of distribution, reduction in the population abundance, and partial displacement, of native and functionally similar species, and interbreeding with them (reviewed in van Lenteren et al. 2006). One of the most famous cases is that of Harmonia axyridis, a coccinellid predator of Asian origin that caused important environmental damage in North America (reviewed in Koch & Galvan, 2008).
Fortunately, after the implementation of the Nagoya protocol (CBD, 2011) importation of exotic species for BPC use was severely restricted and controlled, worldwide. Consequently, companies and agricultural scientist were driven to reinforce their focus and interest on the exploitation of native natural enemies, via the mass-rearing and release of native candidates (augmentative BPC), the conservation of landscapes near the crops to provide resources for natural enemies (i.e. conservation biological pest control), or via the exploitation of the genetic variability of BCAs, to create strains performing better at regulating pest populations under specific biotic or abiotic negative circumstances. Some of these cases are cited in Lartigue et al. (2020). The genetic improvement of BCAs is a strategy still in its infancy, but there is no doubt that the interest for it has significantly increased over the last 5 years (Lommen et al 2017, Bielza 2020, Leung et al 2020).
In my humble opinion, what makes the paper of Lartigue et al. (2020) a remarkable contribution to the field of genetic breeding of BCAs is that it opens a new window of opportunities to the field, by exploring the possibilities for artificial selection of behavioral traits (Réale et al. 2007) to "create" strains of natural enemies displaying behavioral syndromes (Sih et al. 2004) that makes them better at regulating pest populations. The behavioral approach for breeding BCAs can then be extended by crossing it with known abiotic and/or biotic hostile environments (e.g. warm and drought environments, presence of predators/competitors to the BCA, respectively) and engineer strains more prompt to display particular behavioral syndromes to help them to overcome the overall hostility of specific environments. I strongly believe that the approach proposed in Lartigue et al. (2020) will influence the future management of agricultural systems, where strategies including the genetic breeding of BCAs’ behavior will contribute to create better guards and protectors of our crops.

References

Bielza, P., Balanza, V., Cifuentes, D. and Mendoza, J. E. (2020). Challenges facing arthropod biological control: Identifying traits for genetic improvement of predators in protected crops. Pest Manag Sci. doi: https://doi.org/10.1002/ps.5857
CBD - Convention on Biological Diversity, 2011. The Nagoya Protocol on Access and Benefit-sharing, https://www.cbd.int/abs/doc/protocol/nagoya-protocol-en.pdf
Hörstadius, S. (1974). Linnaeus, animals and man. Biological Journal of the Linnaean Society, 6, 269-275. doi: https://doi.org/10.1111/j.1095-8312.1974.tb00725.x
Koch, R.L. and Galvan, T.L. (2008). Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53, 23–35. doi: https://doi.org/10.1007/978-1-4020-6939-0_3
Konishi, M. and Ito, Y. (1973). Early entomology in East Asia. In: Smith, R.F., Mittler, T.E., Smith, C.N. (Eds.), History of Entomology, Annual Reviews Inc., Palo Alto, California, pp. 1-20.
Lartigue, S., Yalaoui, M., Belliard, J., Caravel, C., Jeandroz, L., Groussier, G., Calcagno, V., Louâpre, P., Dechaume-Moncharmont, F.-X., Malausa, T. and Moreau, J. (2020). Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case study. bioRxiv, 2020.08.21.257881, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.08.21.257881
Leung et al. (2020). Next-generation biological control: the need for integrating genetics and genomics. Biological Reviews, 95(6), 1838–1854. doi: https://doi.org/10.1111/brv.12641
Lommen, S. T. E., de Jong, P. W. and Pannebakker, B. A. (2017). It is time to bridge the gap between exploring and exploiting: prospects for utilizing intraspecific genetic variation to optimize arthropods for augmentative pest control – a review. Entomologia Experimentalis et Applicata, 162: 108-123. doi: https://doi.org/10.1111/eea.12510
Réale, D., Reader, S. M., Sol, D., McDougall, P. T. and Dingemanse, N. J. (2007). Integrating animal temperament within ecology and evolution. Biological Reviews, 82: 291-318. doi: https://doi.org/10.1111/j.1469-185X.2007.00010.x
Sih, A., Bell, A. and Johnson, J. C. (2004). Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology and Evolution, 19(7), 372–378. doi: https://doi.org/10.1016/j.tree.2004.04.009
UUNN. 2015. Transforming our world: the 2030 Agenda for Sustainable Development. report of the Open Working Group of the General Assembly on Sustainable Development Goals (A/68/970 and Corr.1; see also A/68/970/Add.1–3).
UUNN. 2019. World population prospects 2019. United Nations, Department of Economic and Social Affairs, Population Division: Highlights. ST/ESA/SER.A/423.
van Lenteren, J. C., Bale, J., Bigler, F., Hokkanen, H. M. T. and Loomans A. J. M. (2006). Assessing risks of releasing exotic biological control agents of arthropod pests. Annual Review of Entomology, 51: 609-634. doi: https://doi.org/10.1146/annurev.ento.51.110104.151129

Consistent variations in personality traits and their potential for genetic improvement of biocontrol agents: Trichogramma evanescens as a case studySilène Lartigue, Myriam Yalaoui, Jean Belliard, Claire Caravel, Louise Jeandroz, Géraldine Groussier, Vincent Calcagno, Philippe Louâpre, François-Xavier Dechaume-Moncharmont, Thibaut Malausa and Jérôme Moreau<p>Improvements in the biological control of agricultural pests require improvements in the phenotyping methods used by practitioners to select efficient biological control agent (BCA) populations in industrial rearing or field conditions. Consist...Agroecology, Behaviour & Ethology, Biological control, Evolutionary ecology, Life historyMarta Montserrat2020-08-24 10:40:03 View
01 Mar 2019
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Parasite intensity is driven by temperature in a wild bird

The global change of species interactions

Recommended by based on reviews by 2 anonymous reviewers

What kinds of studies are most needed to understand the effects of global change on nature? Two deficiencies stand out: lack of long-term studies [1] and lack of data on species interactions [2]. The paper by Mennerat and colleagues [3] is particularly valuable because it addresses both of these shortcomings. The first one is obvious. Our understanding of the impact of climate on biota improves with longer times series of observations. Mennerat et al. [3] analysed an impressive 18-year series from multiple sites to search for trends in parasitism rates across a range of temperatures. The second deficiency (lack of species interaction data) is perhaps not yet fully appreciated, despite studies pointing this out ten years ago [2,4]. The focus is often on species range limits and how taking species interactions into account changes species range predictions based on climate alone (climate envelope models; [5]). But range limits are not everything, as the function of a species (or community, network, etc.) ultimately depends on the strengths of species interactions and not only on the presence or absence of a given species [2,4]. Mennerat et al. [3] show that in the case of birds and their nest parasites, it is the strength of the interaction that has changed, while the species involved stayed the same. Mennerat et al. [3] found nest parasitism to increase with temperature at the nestling stage. They have also searched for trends of parasitism dynamics dependence on the host, but did not find any, probably because the nest parasites are generalists and attack other bird species within the study sites. This study thus draws attention to wider networks of interacting species, and we urgently need more data to predict how interaction networks will rewire with progressing environmental change [6,7].

References

[1] Lindenmayer, D.B., Likens, G.E., Andersen, A., Bowman, D., Bull, C.M., Burns, E., et al. (2012). Value of long-term ecological studies. Austral Ecology, 37(7), 745–57. doi: 10.1111/j.1442-9993.2011.02351.x
[2] Tylianakis, J.M., Didham, R.K., Bascompte, J. & Wardle, D.A. (2008). Global change and species interactions in terrestrial ecosystems. Ecology Letters, 11(12), 1351–63. doi: 10.1111/j.1461-0248.2008.01250.x
[3] Mennerat, A., Charmantier, A., Hurtrez-Bousses, S., Perret, P. & Lambrechts, M.M. (2019). Parasite intensity is driven by temperature in a wild bird. bioRxiv, 323311. Ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/323311
[4] Gilman, S.E., Urban, M.C., Tewksbury, J., Gilchrist, G.W. & Holt, R.D. (2010). A framework for community interactions under climate change. Trends in Ecology & Evolution, 25(6), 325–31. doi: 10.1016/j.tree.2010.03.002
[5] Louthan, A.M., Doak, D.F. & Angert, A.L. (2015). Where and when do species interactions set range limits? Trends in Ecology & Evolution, 30(12), 780–92. doi: 10.1016/j.tree.2015.09.011
[6] Bartley, T.J., McCann, K.S., Bieg, C., Cazelles, K., Granados, M., Guzzo, M.M., et al. (2019). Food web rewiring in a changing world. Nature Ecology & Evolution, 3(3), 345–54. doi: 10.1038/s41559-018-0772-3
[7] Staniczenko, P.P.A., Lewis, O.T., Jones, N.S. & Reed-Tsochas, F. (2010). Structural dynamics and robustness of food webs. Ecology Letters, 13(7), 891–9. doi: 10.1111/j.1461-0248.2010.01485.x

Parasite intensity is driven by temperature in a wild birdAdèle Mennerat, Anne Charmantier, Sylvie Hurtrez-Boussès, Philippe Perret, Marcel M Lambrechts<p>Increasing awareness that parasitism is an essential component of nearly all aspects of ecosystem functioning, as well as a driver of biodiversity, has led to rising interest in the consequences of climate change in terms of parasitism and dise...Climate change, Evolutionary ecology, Host-parasite interactions, Parasitology, ZoologyJan Hrcek2018-05-17 14:37:14 View
13 Mar 2021
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Investigating sex differences in genetic relatedness in great-tailed grackles in Tempe, Arizona to infer potential sex biases in dispersal

Dispersal: from “neutral” to a state- and context-dependent view

Recommended by based on reviews by 2 anonymous reviewers

Traditionally, dispersal has often been seen as “random” or “neutral” as Lowe & McPeek (2014) have put it. This simplistic view is likely due to dispersal being intrinsically difficult to measure empirically as well as “random” dispersal being a convenient simplifying assumption in theoretical work. Clobert et al. (2009), and many others, have highlighted how misleading this assumption is. Rather, dispersal seems to be usually a complex reaction norm, depending both on internal as well as external factors. One such internal factor is the sex of the dispersing individual. A recent review of the theoretical literature (Li & Kokko 2019) shows that while ideas explaining sex-biased dispersal go back over 40 years this state-dependency of dispersal is far from comprehensively understood.

Sevchik et al. (2021) tackle this challenge empirically in a bird species, the great-tailed grackle. In contrast to most bird species, where females disperse more than males, the authors report genetic evidence indicating male-biased dispersal. The authors argue that this difference can be explained by the great-tailed grackle’s social and mating-system.

Dispersal is a central life-history trait (Bonte & Dahirel 2017) with major consequences for ecological and evolutionary processes and patterns. Therefore, studies like Sevchik et al. (2021) are valuable contributions for advancing our understanding of spatial ecology and evolution. Importantly, Sevchik et al. also lead to way to a more open and reproducible science of ecology and evolution. The authors are among the pioneers of preregistering research in their field and their way of doing research should serve as a model for others.

References

Bonte, D. & Dahirel, M. (2017) Dispersal: a central and independent trait in life history. Oikos 126: 472-479. doi: https://doi.org/10.1111/oik.03801

Clobert, J., Le Galliard, J. F., Cote, J., Meylan, S. & Massot, M. (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol. Lett.: 12, 197-209. doi: https://doi.org/10.1111/j.1461-0248.2008.01267.x

Li, X.-Y. & Kokko, H. (2019) Sex-biased dispersal: a review of the theory. Biol. Rev. 94: 721-736. doi: https://doi.org/10.1111/brv.12475

Lowe, W. H. & McPeek, M. A. (2014) Is dispersal neutral? Trends Ecol. Evol. 29: 444-450. doi: https://doi.org/10.1016/j.tree.2014.05.009

Sevchik, A., Logan, C. J., McCune, K. B., Blackwell, A., Rowney, C. & Lukas, D. (2021) Investigating sex differences in genetic relatedness in great-tailed grackles in Tempe, Arizona to infer potential sex biases in dispersal. EcoEvoRxiv, osf.io/t6beh, ver. 5 peer-reviewed and recommended by Peer community in Ecology. doi: https://doi.org/10.32942/osf.io/t6beh

Investigating sex differences in genetic relatedness in great-tailed grackles in Tempe, Arizona to infer potential sex biases in dispersalSevchik, A., Logan, C. J., McCune, K. B., Blackwell, A., Rowney, C. and Lukas, D<p>In most bird species, females disperse prior to their first breeding attempt, while males remain closer to the place they hatched for their entire lives. Explanations for such female bias in natal dispersal have focused on the resource-defense ...Behaviour & Ethology, Dispersal & Migration, ZoologyEmanuel A. Fronhofer2020-08-24 17:53:06 View
12 Oct 2020
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Insect herbivory on urban trees: Complementary effects of tree neighbours and predation

Tree diversity is associated with reduced herbivory in urban forest

Recommended by and based on reviews by Ian Pearse and Freerk Molleman

Urban ecology, the study of ecological systems in our increasingly urbanized world, is crucial to planning and redesigning cities to enhance ecosystem services (Kremer et al. 2016), human health and well-being and further conservation goals (Dallimer et al. 2012). Urban trees are a crucial component of urban streets and parks that provide shade and cooling through evapotranspiration (Fung and Jim 2019), improve air quality (Lai and Kontokosta 2019), help control storm water (Johnson and Handel 2016), and conserve wildlife (Herrmann et al. 2012; de Andrade et al. 2020).
Ideally, management of urban forests strikes a balance between maintaining the health of urban trees while retaining those organisms, such as herbivores, that connect a tree to the urban ecosystem. Herbivory by arthropods can substantially affect tree growth and reproduction (Whittaker and Warrington 1985), and so understanding factors that influence herbivory in urban forests is important to effective management. At the same time, herbivorous arthropods are important as key components of urban bird diets (Airola and Greco 2019) and provide a backyard glimpse at forest ecosystems in an increasingly built environment (Pearse 2019). Maintenance of arthropod predators may be one way to retain arthropods in urban forests while keeping detrimental outbreaks of herbivores in check. In “Insect herbivory on urban trees: Complementary effects of tree neighbors and predation” Stemmelen and colleagues (Stemmelen et al. 2020) use a clever sampling design to show that insect herbivory decreases as the diversity of neighboring trees increased. By placing artificial larvae out on trees, they provide evidence that increased predation in higher diversity urban forest patches might drive patterns in herbivory. The paper also demonstrates the importance of tree species identity in determining leaf herbivory.
The implications of this research for urban foresters is that deliberately planting diverse urban forests will help manage insect herbivores and should thus improve tree health. Potential knock-on effects could be seen for the ecosystem services provided by urban forests. While it might be tempting to simply plant more of the species that are subject to low current rates of herbivory, other research on the long-term vulnerability of monocultures to attack by specialist pathogens and herbivores (Tooker and Frank 2012) cautions against such an approach. Furthermore, the importance of urban forest insects to birds, including migrating birds, argues for managing urban forests more holistically (Greco and Airola 2018).
Stemmelen et al. (2020) used an observational approach focused on urban forests in Montreal, Canada in their research. Their findings suggest follow-up research focused on a broader cross-section of urban forests across latitudes, as well as experimental research. Experiments could, for example, exclude avian predators with netting (e.g. (Marquis and Whelan 1994)) to evaluate the relative importance of birds to managing urban insects on trees, as well as the flip side of that equation, the important to birds of insects on urban trees.
In summary, Stemmelen and colleague’s manuscript illustrates clever sampling and use of observational data to infer broader ecological patterns. It is worth reading to better understand the role of diversity in driving plant-insect community interactions and given the implications of the findings for sustainable long-term management of urban forests.

References

Airola, D. and Greco, S. (2019). Birds and oaks in California’s urban forest. Int. Oaks, 30, 109–116.
de Andrade, A.C., Medeiros, S. and Chiarello, A.G. (2020). City sloths and marmosets in Atlantic forest fragments with contrasting levels of anthropogenic disturbance. Mammal Res., 65, 481–491. doi: https://doi.org/10.1007/s13364-020-00492-0
Dallimer, M., Irvine, K.N., Skinner, A.M.J., Davies, Z.G., Rouquette, J.R., Maltby, L.L., et al. (2012). Biodiversity and the Feel-Good Factor: Understanding Associations between Self-Reported Human Well-being and Species Richness. Bioscience, 62, 47–55. doi: https://doi.org/10.1525/bio.2012.62.1.9
Fung, C.K.W. and Jim, C.Y. (2019). Microclimatic resilience of subtropical woodlands and urban-forest benefits. Urban For. Urban Green., 42, 100–112. doi: https://doi.org/10.1016/j.ufug.2019.05.014
Greco, S.E. and Airola, D.A. (2018). The importance of native valley oaks (Quercus lobata) as stopover habitat for migratory songbirds in urban Sacramento, California, USA. Urban For. Urban Green., 29, 303–311. doi: https://doi.org/10.1016/j.ufug.2018.01.005
Herrmann, D.L., Pearse, I.S. and Baty, J.H. (2012). Drivers of specialist herbivore diversity across 10 cities. Landsc. Urban Plan., 108, 123–130. doi: https://doi.org/10.1016/j.landurbplan.2012.08.007
Johnson, L.R. and Handel, S.N. (2016). Restoration treatments in urban park forests drive long-term changes in vegetation trajectories. Ecol. Appl., 26, 940–956. doi: https://doi.org/10.1890/14-2063
Kremer, P., Hamstead, Z., Haase, D., McPhearson, T., Frantzeskaki, N., Andersson, E., et al. (2016). Key insights for the future of urban ecosystem services research. Ecol. Soc., 21: 29. doi: http://doi.org/10.5751/ES-08445-210229
Lai, Y. and Kontokosta, C.E. (2019). The impact of urban street tree species on air quality and respiratory illness: A spatial analysis of large-scale, high-resolution urban data. Heal. Place, 56, 80–87. doi: https://doi.org/10.1016/j.healthplace.2019.01.016
Marquis, R.J. and Whelan, C.J. (1994). Insectivorous birds increase growth of white oak through consumption of leaf-chewing insects. Ecology, 75, 2007–2014. doi: https://doi.org/10.2307/1941605
Pearse, I.S. (2019). Insect herbivores on urban native oak trees. Int. Oaks, 30, 101–108.
Stemmelen, A., Paquette, A., Benot, M.-L., Kadiri, Y., Jactel, H. and Castagneyrol, B. (2020) Insect herbivory on urban trees: Complementary effects of tree neighbours and predation. bioRxiv, 2020.04.15.042317, ver. 5 peer-reviewed and recommended by PCI Ecology. doi: https://doi.org/10.1101/2020.04.15.042317
Tooker, J. F., and Frank, S. D. (2012). Genotypically diverse cultivar mixtures for insect pest management and increased crop yields. J. Appl. Ecol., 49(5), 974-985. doi: https://doi.org/10.1111/j.1365-2664.2012.02173.x
Whittaker, J.B. and Warrington, S. (1985). An experimental field study of different levels of insect herbivory induced By Formica rufa predation on Sycamore (Acer pseudoplatanus) III. Effects on Tree Growth. J. Appl. Ecol., 22, 797. doi: https://doi.org/10.2307/2403230

Insect herbivory on urban trees: Complementary effects of tree neighbours and predationAlex Stemmelen, Alain Paquette, Marie-Lise Benot, Yasmine Kadiri, Hervé Jactel, Bastien Castagneyrol<p>Insect herbivory is an important component of forest ecosystems functioning and can affect tree growth and survival. Tree diversity is known to influence insect herbivory in natural forest, with most studies reporting a decrease in herbivory wi...Biodiversity, Biological control, Community ecology, Ecosystem functioning, HerbivoryRuth Arabelle Hufbauer2020-04-20 13:49:36 View
07 Oct 2019
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Deer slow down litter decomposition by reducing litter quality in a temperate forest

Disentangling effects of large herbivores on litter decomposition

Recommended by based on reviews by 2 anonymous reviewers

Aboveground – belowground interactions is a fascinating field that has developed in ecology since about 20 years [1]. This field has been very fruitful as measured by the numerous articles published but also by the particular role it has played in the development of soil ecology. While soil ecology has for a long time developed partially independently from “general ecology” [2], the field of aboveground – belowground interactions has shown that all ecological interactions occurring within the soil are likely to impact plant growth and plant physiology because they have their roots within the soil. In turns, this should impact the aerial system of plants (higher or lower biomasses, changes in leaf quality…), which should cascade on the aboveground food web. Conversely, all ecological interactions occurring aboveground likely impact plant growth, which should cascade to their root systems, and thus to the soil functioning and the soil food web (through changes in the emission of exudates or inputs of dead roots…). Basically, plants are linking the belowground and aboveground worlds because, as terrestrial primary producers, they need to have (1) leaves to capture CO2 and exploit light and (2) roots to absorb water and mineral nutrients. The article I presently recommend [3] tackles this general issue through the prism of the impact of large herbivores on the decomposition of leaf litter.
This issue is a relatively old one [4, 5] but still deserves efforts because there have been relatively few studies on the subject and because the issue is relatively complex due to the diversity of mechanisms involved and the difficulty to disentangle them. I recommend this article because the authors have cleverly taken advantage of a ‘‘natural’’ long-term experiment, i.e. three islands with contrasted deer densities, to test whether these large mammals are able to impact leaf litter decomposition and whether they are able to do so through changes in litter quality (because they browse the vegetation) or through changes in soil characteristics (either physical or chemical characteristics or the composition of the decomposer community). They have found that deer decrease litter decomposition, mainly through a decrease in litter quality (increase in its C:N ratio). I particularly appreciate the combination of statistics achieved to test the different hypotheses and the fair and in-depth discussion of the results.
I have to confess that I have two small regrets with this work. First, all replications are implemented within the same three islands, so that it cannot be fully excluded that measured effects should not be attributed to any other possible difference between the three islands. I am fairly sure this is not the case (at least because the three islands have the same environments) but I hope that future studies or meta-analyses will be able analyse independent deer density treatments. Second, as a soil ecologist, I am eager to see results on the decomposer communities, both microorganisms and macrofauna, of the three islands.

References

[1] Hooper, D. U., Bignell, D. E., Brown, V. K., Brussard, L., Dangerfield, J. M., Wall, D. H. and Wolters, V. (2000). Interactions between Aboveground and Belowground Biodiversity in Terrestrial Ecosystems: Patterns, Mechanisms, and Feedbacks. BioScience, 50(12), 1049-1061. doi: 10.1641/0006-3568(2000)050[1049:ibaabb]2.0.co;2
[2] Barot, S., Blouin, M., Fontaine, S., Jouquet, P., Lata, J.-C., and Mathieu, J. (2007). A Tale of Four Stories: Soil Ecology, Theory, Evolution and the Publication System. PLOS ONE, 2(11), e1248. doi: 10.1371/journal.pone.0001248
[3] Chollet S., Maillard M., Schörghuber J., Grayston S. and Martin J.-L. (2019). Deer slow down litter decomposition by reducing litter quality in a temperate forest. bioRxiv, 690032, ver. 3 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/690032
[4] Wardle, D. A., Barker, G. M., Yeates, G. W., Bonner, K. I., and Ghani, A. (2001). Introduced browsing mammals in New Zealand natural forests: aboveground and belowground consequences. Ecological Monographs, 71(4), 587-614. doi: 10.1890/0012-9615(2001)071[0587:ibminz]2.0.co;2
[5] Bardgett, R. D., and Wardle, D. A. (2003). Herbivore-mediated linkages between aboveground and belowground communities. Ecology, 84(9), 2258-2268. doi: 10.1890/02-0274

Deer slow down litter decomposition by reducing litter quality in a temperate forest Simon Chollet, Morgane Maillard, Juliane Schorghuber, Sue Grayston, Jean-Louis Martin<p>In temperate forest ecosystems, the role of deer in litter decomposition, a key nutrient cycling process, remains debated. Deer may modify the decomposition process by affecting plant cover and thus modifying litter abundance. They can also alt...Community ecology, Ecosystem functioning, Herbivory, Soil ecologySébastien Barot2019-07-04 14:30:19 View
16 Jun 2020
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Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework

Stasis and the phenotypic gambit

Recommended by based on reviews by Jacob Johansson, Katja Räsänen and 1 anonymous reviewer

The preprint "Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework" by Coulson (2020) presents a general framework for evolutionary ecology, useful to interpret patterns of selection and evolutionary responses to environmental transitions. The paper is written in an accessible and intuitive manner. It reviews important concepts which are at the heart of evolutionary ecology. Together, they serve as a worldview which you can carry with you to interpret patterns in data or observations in nature. I very much appreciate it that Coulson (2020) presents his personal intuition laid bare, the framework he uses for his research and how several strong concepts from theoretical ecology fit in there. Overviews as presented in this paper are important to understand how we as researchers put the pieces together.
A main message of the paper is that resource detection and acquisition traits, broadly called "resource accrual traits" are at the core of evolutionary dynamics. These traits and the processes they are involved in often urge some degree of individual specialization. Not all traits are resource accrual traits all the time. Guppies are cited as an example, which have traits in high predation environments that make foraging easier for them, such as being less conspicuous to predators. In the absence of predators, these same traits might be neutral. Their colour pattern might then contribute much less to the odds of obtaining resources.
"Resource accrual" reminds me of discussions of resource holding potential (Parker 1974), which can be for example the capacity to remain on a bird feeder without being dislodged. However, the idea is much broader and aggression does not need to be important for the acquisition of resources. Evolutionary success is reserved for those steadily obtaining resources. This recalls the pessimization principle of Metz et al. (2008), which applies in a restricted set of situations and where the strategy which persists at the lowest resource levels systematically wins evolutionary contests. If this principle would apply universally, the world then inherently become the worst possible. Resources determine energy budgets and different life history strategies allocate these differently to maximize fitness. The fine grain of environments and the filtration by individual histories generate a lot of variation in outcomes. However, constraint-centered approaches (Kempes et al. 2019, Kooijman 2010) are mentioned but are not at the core of this preprint. Evolution is rather seen as dynamic programming optimization with interactions within and between species. Coulson thus extends life history studies such as for example Tonnabel et al. (2012) with eco-evolutionary feedbacks. Examples used are guppies, algae-rotifer interactions and others. Altogether, this makes for an optimistic paper pushing back the pessimization principle.
Populations are expected to spend most of the time in quasi-equilibrium states where the long run stochastic growth rate is close to zero for all genotypes, alleles or other chosen classes. In the preprint, attention is given to reproductive value calculus, another strong tool in evolutionary dynamics (Grafen 2006, Engen et al. 2009), which tells us how classes within a population contribute to population composition in the distant future. The expected asymptotic fitness of an individual is equated to its expected reproductive value, but this might require particular ways of calculating reproductive values (Coulson 2020). Life history strategies can also be described by per generation measures such as R0 (currently on everyone's radar due to the coronavirus pandemic), generation time etc. Here I might disagree because I believe that this focus in per generation measures can lead to an incomplete characterization of plastic and other strategies involved in strategies such as bet-hedging. A property at quasi-equilibrium states is precise enough to serve as a null hypothesis which can be falsified: all types must in the long run leave equal numbers of descendants. If there is any property in evolutionary ecology which is useful it is this one and it rightfully merits attention.
However, at quasi-equilibrium states, directional selection has been observed, often without the expected evolutionary response. The preprint aims to explain this and puts forward the presence of non-additive gene action as a mechanism. I don't believe that it is the absence of clonal inheritance which matters very much in itself (Van Dooren 2006) unless genes with major effect are present in protected polymorphisms. The preprint remains a bit unclear on how additive gene action is broken, and here I add from the sphere in which I operate. Non-additive gene action can be linked to non-linear genotype-phenotype maps (Van Dooren 2000, Gilchrist and Nijhout 2001) and if these maps are non-linear enough to create constraints on phenotype determination, by means of maximum or minimum phenotypes which cannot be surpassed for any combination of the underlying traits, then they create additional evolutionary quasi-equilibrium states, with directional selection on a phenotype such as body size. I believe Coulson hints at this option (Coulson et al. 2006), but also at a different one: if body size is mostly determined by variation in resource accrual traits, then the resource accrual traits can be under stabilizing selection while body size is not. This requires that all resource accrual traits affect other phenotypic or demographic properties next to body size. In both cases, microevolutionary outcomes cannot be inferred from inspecting body sizes alone, either resource accrual traits need to be included explicitly, or non-linearities, or both when the map between resource accrual and body size is non-linear (Van Dooren 2000).
The discussion of the phenotypic gambit (Grafen 1984) leads to another long-standing issue in evolutionary biology. Can predictions of adaptation be made by inspecting and modelling individual phenotypes alone? I agree that with strongly non-linear genotype-phenotype maps they cannot and for multivariate sets of traits, genetic and phenotypic correlations can be very different (Hadfield et al. 2007). However, has the phenotypic gambit ever claimed to be valid globally or should it rather be used locally for relatively small amounts of variation? Grafen (1984) already contained caveats which are repeated here. As a first approximation, additivity might produce quite correct predictions and thus make the gambit operational in many instances. When important individual traits are omitted, it may just be misspecified. I am interested to see cases where the framework Coulson (2020) proposes is used for very large numbers of phenotypic and genotypic attributes. In the end, these highly dimensional trait distributions might basically collapse to a few major axes of variation due to constraints on resource accrual.
I highly recommend reading this preprint and I am looking forward to the discussion it will generate.

References

[1] Coulson, T. (2020) Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback framework. bioRxiv, 509067, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/509067
[2] Coulson, T., Benton, T. G., Lundberg, P., Dall, S. R. X., and Kendall, B. E. (2006). Putting evolutionary biology back in the ecological theatre: a demographic framework mapping genes to communities. Evolutionary Ecology Research, 8(7), 1155-1171.
[3] Engen, S., Lande, R., Sæther, B. E. and Dobson, F. S. (2009) Reproductive value and the stochastic demography of age-structured populations. The American Naturalist 174: 795-804. doi: 10.1086/647930
[4] Gilchrist, M. A. and Nijhout, H. F. (2001). Nonlinear developmental processes as sources of dominance. Genetics, 159(1), 423-432.
[5] Grafen, A. (1984) Natural selection, kin selection and group selection. In: Behavioural Ecology: An Evolutionary Approach,2nd edn (JR Krebs & NB Davies eds), pp. 62–84. Blackwell Scientific, Oxford.
[6] Grafen, A. (2006). A theory of Fisher's reproductive value. Journal of mathematical biology, 53(1), 15-60. doi: 10.1007/s00285-006-0376-4
[7] Hadfield, J. D., Nutall, A., Osorio, D. and Owens, I. P. F. (2007). Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. Journal of evolutionary biology, 20(2), 549-557. doi: 10.1111/j.1420-9101.2006.01262.x
[8] Kempes, C. P., West, G. B., and Koehl, M. (2019). The scales that limit: the physical boundaries of evolution. Frontiers in Ecology and Evolution, 7, 242. doi: 10.3389/fevo.2019.00242
[9] Kooijman, S. A. L. M. (2010) Dynamic Energy Budget theory for metabolic organisation. University Press, third edition.
[10] Metz, J. A. J., Mylius, S.D. and Diekman, O. (2008) When does evolution optimize?. Evolutionary Ecology Research 10: 629-654.
[11] Parker, G. A. (1974). Assessment strategy and the evolution of fighting behaviour. Journal of theoretical Biology, 47(1), 223-243. doi: 10.1016/0022-5193(74)90111-8
[12] Tonnabel, J., Van Dooren, T. J. M., Midgley, J., Haccou, P., Mignot, A., Ronce, O., and Olivieri, I. (2012). Optimal resource allocation in a serotinous non‐resprouting plant species under different fire regimes. Journal of Ecology, 100(6), 1464-1474. doi: 10.1111/j.1365-2745.2012.02023.x
[13] Van Dooren, T. J. M. (2000). The evolutionary dynamics of direct phenotypic overdominance: emergence possible, loss probable. Evolution, 54(6), 1899-1914. doi: 10.1111/j.0014-3820.2000.tb01236.x
[14] Van Dooren, T. J. M. (2006). Protected polymorphism and evolutionary stability in pleiotropic models with trait‐specific dominance. Evolution, 60(10), 1991-2003. doi: 10.1111/j.0014-3820.2006.tb01837.x

Environmental perturbations and transitions between ecological and evolutionary equilibria: an eco-evolutionary feedback frameworkTim Coulson<p>I provide a general framework for linking ecology and evolution. I start from the fact that individuals require energy, trace molecules, water, and mates to survive and reproduce, and that phenotypic resource accrual traits determine an individ...Eco-evolutionary dynamics, Evolutionary ecologyTom Van Dooren2019-01-03 10:05:16 View
06 Oct 2020
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Implementing a rapid geographic range expansion - the role of behavior and habitat changes

The role of behavior and habitat availability on species geographic expansion

Recommended by ORCID_LOGO based on reviews by Caroline Marie Jeanne Yvonne Nieberding, Pizza Ka Yee Chow, Tim Parker and 1 anonymous reviewer

Understanding the relative importance of species-specific traits and environmental factors in modulating species distributions is an intriguing question in ecology [1]. Both behavioral flexibility (i.e., the ability to change the behavior in changing circumstances) and habitat availability are known to influence the ability of a species to expand its geographic range [2,3]. However, the role of each factor is context and species dependent and more information is needed to understand how these two factors interact. In this pre-registration, Logan et al. [4] explain how they will use Great-tailed grackles (Quiscalus mexicanus), a species with a flexible behavior and a rapid geographic range expansion, to evaluate the relative role of habitat and behavior as drivers of the species’ expansion [4]. The authors present very clear hypotheses, predicted results and also include alternative predictions. The rationales for all the hypotheses are clearly stated, and the methodology (data and analyses plans) are described with detail. The large amount of information already collected by the authors for the studied species during previous projects warrants the success of this study. It is also remarkable that the authors will make all their data available in a public repository, and that the pre-registration in already stored in GitHub, supporting open access and reproducible science. I agree with the three reviewers of this pre-registration about its value and I think its quality has largely improved during the review process. Thus, I am happy to recommend it and I am looking forward to seeing the results.

References

[1] Gaston KJ. 2003. The structure and dynamics of geographic ranges. Oxford series in Ecology and Evolution. Oxford University Press, New York.

[2] Sol D, Lefebvre L. 2000. Behavioural flexibility predicts invasion success in birds introduced to new zealand. Oikos. 90(3): 599–605. https://doi.org/10.1034/j.1600-0706.2000.900317.x

[3] Hanski I, Gilpin M. 1991. Metapopulation dynamics: Brief history and conceptual domain. Biological journal of the Linnean Society. 42(1-2): 3–16. https://doi.org/10.1111/j.1095-8312.1991.tb00548.x

[4] Logan CJ, McCune KB, Chen N, Lukas D. 2020. Implementing a rapid geographic range expansion - the role of behavior and habitat changes (http://corinalogan.com/Preregistrations/gxpopbehaviorhabitat.html) In principle acceptance by PCI Ecology of the version on 16 Dec 2021 https://github.com/corinalogan/grackles/blob/0fb956040a34986902a384a1d8355de65010effd/Files/Preregistrations/gxpopbehaviorhabitat.Rmd.

Implementing a rapid geographic range expansion - the role of behavior and habitat changesLogan CJ, McCune KB, Chen N, Lukas D<p>It is generally thought that behavioral flexibility, the ability to change behavior when circumstances change, plays an important role in the ability of a species to rapidly expand their geographic range (e.g., Lefebvre et al. (1997), Griffin a...Behaviour & Ethology, Biological invasions, Dispersal & Migration, Foraging, Habitat selection, Human impact, Phenotypic plasticity, Preregistrations, ZoologyEsther Sebastián GonzálezAnonymous, Caroline Marie Jeanne Yvonne Nieberding, Tim Parker2020-05-14 11:18:57 View
28 Aug 2023
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Implementing a rapid geographic range expansion - the role of behavior changes

Behavioral changes in the rapid geographic expansion of the great-tailed grackle

Recommended by ORCID_LOGO based on reviews by Francois-Xavier Dechaume-Moncharmont, Pizza Ka Yee Chow and 1 anonymous reviewer

While many species' populations are declining, primarily due to human-related impacts (McKnee et al., 2014), certain species have thrived by utilizing human-influenced environments, leading to their population expansion (Muñoz & Real, 2006). In this context, the capacity to adapt and modify behaviors in response to new surroundings is believed to play a crucial role in facilitating species' spread to novel areas (Duckworth & Badyaev, 2007). For example, an increase in innovative behaviors within recently established communities could aid in discovering previously untapped food resources, while a decrease in exploration might reduce the likelihood of encountering dangers in unfamiliar territories (e.g., Griffin et al., 2016). To investigate the contribution of these behaviors to rapid range expansions, it is essential to directly measure and compare behaviors in various populations of the species.

The study conducted by Logan et al. (2023) aims to comprehend the role of behavioral changes in the range expansion of great-tailed grackles (Quiscalus mexicanus). To achieve this, the researchers compared the prevalence of specific behaviors at both the expansion's edge and its middle. Great-tailed grackles were chosen as an excellent model due to their behavioral adaptability, rapid geographic expansion, and their association with human-modified environments. The authors carried out a series of experiments in captivity using wild-caught individuals, following a detailed protocol. The study successfully identified differences in two of the studied behavioral traits: persistence (individuals participated in a larger proportion of trials) and flexibility variance (a component of the species' behavioral flexibility, indicating a higher chance that at least some individuals in the population could be more flexible). Notably, individuals at the edge of the population exhibited higher values of persistence and flexibility, suggesting that these behavioral traits might be contributing factors to the species' expansion. Overall, the study by Logan et al. (2023) is an excellent example of the importance of behavioral flexibility and other related behaviors in the process of species' range expansion and the significance of studying these behaviors across different populations to gain a better understanding of their role in the expansion process.

Finally, it is important to underline that this study is part of a pre-registration that received an In Principle Recommendation in PCI Ecology (Sebastián-González 2020) where objectives, methodology, and expected results were described in detail. The authors have identified any deviation from the original pre-registration and thoroughly explained the reasons for their deviations, which were very clear. 

References

Duckworth, R. A., & Badyaev, A. V. (2007). Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proceedings of the National Academy of Sciences, 104(38), 15017-15022. https://doi.org/10.1073/pnas.0706174104

Griffin, A.S., Guez, D., Federspiel, I., Diquelou, M., Lermite, F. (2016). Invading new environments: A mechanistic framework linking motor diversity and cognition to establishment success. Biological Invasions and Animal Behaviour, 26e46. https://doi.org/10.1017/CBO9781139939492.004

Logan, C. J., McCune, K., LeGrande-Rolls, C., Marfori, Z., Hubbard, J., Lukas, D. 2023. Implementing a rapid geographic range expansion - the role of behavior changes. EcoEvoRxiv, ver. 3 peer-reviewed and recommended by PCI Ecology. https://doi.org/10.32942/X2N30J

McKee, J. K., Sciulli, P. W., Fooce, C. D., & Waite, T. A. (2004). Forecasting global biodiversity threats associated with human population growth. Biological Conservation, 115(1), 161-164. https://doi.org/10.1016/S0006-3207(03)00099-5

Muñoz, A. R., & Real, R. (2006). Assessing the potential range expansion of the exotic monk parakeet in Spain. Diversity and Distributions, 12(6), 656-665. https://doi.org/10.1111/j.1472-4642.2006.00272.x

Sebastián González, E. (2020) The role of behavior and habitat availability on species geographic expansion. Peer Community in Ecology, 100062. https://doi.org/10.24072/pci.ecology.100062. Reviewers: Caroline Nieberding, Tim Parker, and Pizza Ka Yee Chow.

Implementing a rapid geographic range expansion - the role of behavior changesLogan CJ, McCune KB, LeGrande-Rolls C, Marfori Z, Hubbard J, Lukas D<p>It is generally thought that behavioral flexibility, the ability to change behavior when circumstances change, plays an important role in the ability of species to rapidly expand their geographic range. Great-tailed grackles (<em>Quiscalus mexi...Behaviour & Ethology, Preregistrations, ZoologyEsther Sebastián González2023-04-12 11:00:42 View
02 Aug 2022
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The effect of dominance rank on female reproductive success in social mammals

When do dominant females have higher breeding success than subordinates? A meta-analysis across social mammals.

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

In this meta-analysis, Shivani et al. [1] investigate 1) whether dominance and reproductive success are generally associated across social mammals and 2) whether this relationship varies according to a) life history traits (e.g., stronger for species with large litter size), b) ecological conditions (e.g., stronger when resources are limited) and c) the social environment (e.g., stronger for cooperative breeders than for plural breeders). Generally, the results are consistent with their predictions, except there was no clear support for this relationship to be conditional on the ecological conditions. considered

As I have previously recommended the preregistration of this study [2,3], I do not have much to add here, as such recommendation should not depend on the outcome of the study. What I would like to recommend is the whole scientific process performed by the authors, from preregistration sent for peer review, to preprint submission and post-study peer review. It is particularly recommendable to notice that this project was a Masters student project, which shows that it is possible and worthy to preregister studies, even for such rather short-term projects. I strongly congratulate the authors for choosing this process even for an early career short-term project. I think it should be made possible for short-term students to conduct a preregistration study as a research project, without having to present post-study results. I hope this study can encourage a shift in the way we sometimes evaluate students’ projects.

I also recommend the readers to look into the whole pre- and post- study reviewing history of this manuscript and the associated preregistration, as it provides a better understanding of the process and a good example of the associated challenges and benefits [4]. It was a really enriching experience and I encourage others to submit and review preregistrations and registered reports!

 

References

[1] Shivani, Huchard, E., Lukas, D. (2022). The effect of dominance rank on female reproductive success in social mammals. EcoEvoRxiv, rc8na, ver. 10 peer-reviewed and recommended by Peer Community in Ecology. https://doi.org/10.32942/osf.io/rc8na

[2] Shivani, Huchard, E., Lukas, D. (2020). Preregistration - The effect of dominance rank on female reproductive success in social mammals In principle acceptance by PCI Ecology of the version 1.2 on 07 July 2020. https://dieterlukas.github.io/Preregistration_MetaAnalysis_RankSuccess.html

[3] Paquet, M. (2020) Why are dominant females not always showing higher reproductive success? A preregistration of a meta-analysis on social mammals. Peer Community in Ecology, 100056. https://doi.org/10.24072/pci.ecology.100056

[4] Parker, T., Fraser, H., & Nakagawa, S. (2019). Making conservation science more reliable with preregistration and registered reports. Conservation Biology, 33(4), 747-750. https://doi.org/10.1111/cobi.13342

The effect of dominance rank on female reproductive success in social mammalsShivani, Elise Huchard, Dieter Lukas<p>Life in social groups, while potentially providing social benefits, inevitably leads to conflict among group members. In many social mammals, such conflicts lead to the formation of dominance hierarchies, where high-ranking individuals consiste...Behaviour & Ethology, Meta-analysesMatthieu Paquet2021-10-13 18:26:42 View
13 Jul 2020
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Preregistration - The effect of dominance rank on female reproductive success in social mammals

Why are dominant females not always showing higher reproductive success? A preregistration of a meta-analysis on social mammals

Recommended by ORCID_LOGO based on reviews by Bonaventura Majolo and 1 anonymous reviewer

In social species conflicts among group members typically lead to the formation of dominance hierarchies with dominant individuals outcompeting other groups members and, in some extreme cases, suppressing reproduction of subordinates. It has therefore been typically assumed that dominant individuals have a higher breeding success than subordinates. However, previous work on mammals (mostly primates) revealed high variation, with some populations showing no evidence for a link between female dominance reproductive success, and a meta-analysis on primates suggests that the strength of this relationship is stronger for species with a longer lifespan [1]. Therefore, there is now a need to understand 1) whether dominance and reproductive success are generally associated across social mammals (and beyond) and 2) which factors explains the variation in the strength (and possibly direction) of this relationship.
In their preregistration, Shivani et al. [2] plan to perform a meta-analysis on 86 social mammal species to address these two points. More specifically, they will investigate whether the relationship between female dominance and reproductive success vary according to life history traits (e.g. stronger for species with large litter size), ecological conditions (e.g. stronger when resources are limited) and the social environment (e.g. stronger for cooperative breeders than for plural breeders).
The two reviewers and I were particularly positive and enthusiastic about this preregistration and only had minor comments that were nicely addressed by the authors. We found the background well-grounded in the existing literature and that the predictions were therefore clear and well-motivated. The methods were particularly transparent with a nicely annotated R script and the authors even simulated a dataset with the same structure as the actual data in order to make sure that the coding of the data handling and statistical analyses were appropriate (without being tempted to look at model outputs from the true dataset).
Perhaps one limitation to keep in mind once we will have the chance to look at the outcome of this study if that the dataset may not be fully representative of social species with dominance hierarchies. For example, the current dataset contains only one aquatic mammal (Mirounga angustirostris) as far as I can see, which is likely due to a lack of knowledge on such systems. Furthermore, not only mammals exhibit dominance hierarchies and it will be interesting to see if the results of the proposed study hold for other social taxa (and if not, what may explain their differences).
That being said, the proposed study will already offer a much broader overview of the relationship between dominance and reproductive success in animal societies and a better understanding for its variation. The reviewers and I believe it will make an important contribution to the fields of socio-ecology and evolutionary ecology. I therefore strongly recommend this preregistration and we are particularly looking forward to seeing the outcome of this exciting study.

References

[1] Majolo, B., Lehmann, J., de Bortoli Vizioli, A., & Schino, G. (2012). Fitness‐related benefits of dominance in primates. American journal of physical anthropology, 147(4), 652-660. doi: 10.1002/ajpa.22031
[2] Shivani, Huchard, E., Lukas, D. (2020). Preregistration - The effect of dominance rank on female reproductive success in social mammals In principle acceptance by PCI Ecology of the version 1.2 on 07 July 2020. https://github.com/dieterlukas/FemaleDominanceReproductionMetaAnalysis/blob/trunk/PreregistrationMetaAnalysis_RankSuccess.Rmd

Preregistration - The effect of dominance rank on female reproductive success in social mammalsShivani, Elise Huchard, Dieter Lukas<p>Life in social groups, while potentially providing social benefits, inevitably leads to conflict among group members. In many social mammals, such conflicts lead to the formation of dominance hierarchies, where high-ranking individuals consiste...Behaviour & Ethology, Meta-analyses, Preregistrations, Social structure, ZoologyMatthieu Paquet Bonaventura Majolo, Anonymous2020-04-06 17:42:37 View