Section: Evolutionary Biology
Topic: Ecology, Evolution

A gene-regulatory network model for density-dependent and sex-biased dispersal evolution during range expansions

Deshpande, Jhelam N.1, 2  ; Fronhofer, Emanuel A.1  
1 ISEM, Université de Montpellier, CNRS, IRD, EPHE, Montpellier, France
2 Indian Institute of Science Education and Research (IISER) Pune, Pune, Maharashtra, India

Corresponding author(s): Deshpande, Jhelam N. (jndeshpande@ucsd.edu); Fronhofer, Emanuel A. (emanuel.fronhofer@umontpellier.fr)

10.24072/pcjournal.626 - Peer Community Journal, Volume 5 (2025), article no. e127

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Dispersal is key to understanding ecological and evolutionary dynamics. Dispersal may itself evolve and exhibit phenotypic plasticity. Specifically, organisms may modulate their dispersal rates in response to the density of their conspecifics (density-dependent dispersal) and their own sex (sex-biased dispersal). While optimal dispersal plastic responses have been derived from first principles, the genetic and molecular basis of dispersal plasticity has not been modelled. An understanding of the genetic architecture of dispersal plasticity is especially relevant for understanding dispersal evolution during rapidly changing spatial ecological conditions such as range expansions. In this context, we develop an individual-based metapopulation model of the evolution of density-dependent and sex-biased dispersal during range expansions. We represent the dispersal trait as a gene-regulatory network (GRN), which can take population density and an individual's sex as an input and analyse emergent context- and condition-dependent dispersal responses. We compare dispersal evolution and ecological dynamics in this GRN model to a standard reaction norm (RN) approach under equilibrium metapopulation conditions and during range expansions. We find that under equilibrium metapopulation conditions, the GRN model produces emergent density-dependent and sex-biased dispersal plastic response shapes that match the theoretical expectation of the RN model. However, during range expansion, when mutation effects are large enough, the GRN model leads to faster range expansion because GRNs can maintain higher adaptive potential. Our results imply that, in order to understand eco-evolutionary dynamics in contemporary time, the genetic architecture of traits must be taken into account.

Published online:
DOI: 10.24072/pcjournal.626
Type: Research article
Keywords: gene-regulatory network, dispersal, plasticity, range expansion, density-dependent dispersal

Deshpande, Jhelam N. 1, 2; Fronhofer, Emanuel A. 1

1 ISEM, Université de Montpellier, CNRS, IRD, EPHE, Montpellier, France
2 Indian Institute of Science Education and Research (IISER) Pune, Pune, Maharashtra, India
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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Deshpande, J. N.; Fronhofer, E. A. A gene-regulatory network model for density-dependent and sex-biased dispersal evolution during range expansions. Peer Community Journal, Volume 5 (2025), article  no. e127. https://doi.org/10.24072/pcjournal.626

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.evolbiol.100749

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] Alberch, P. From genes to phenotype: dynamical systems and evolvability, Genetica, Volume 84 (1991) no. 1, pp. 5-11 | DOI

[2] Altwegg, R.; Collingham, Y. C.; Erni, B.; Huntley, B. Density-dependent dispersal and the speed of range expansions, Divers. Distrib., Volume 19 (2013) no. 1, pp. 60-68 | DOI

[3] Armenta, T. C.; Cole, S. W.; Geschwind, D. H.; Blumstein, D. T.; Wayne, R. K. Gene expression shifts in yellow-bellied marmots prior to natal dispersal, Behav. Ecol., Volume 30 (2019) no. 2, pp. 267-277 | DOI

[4] Baines, C. B.; Travis, J. M. J.; McCauley, S. J.; Bocedi, G. Negative density-dependent dispersal emerges from the joint evolution of density- and body condition-dependent dispersal strategies, Evolution, Volume 74 (2020) no. 10, pp. 2238-2249 | DOI

[5] Beverton, R. J. H.; Holt, S. J. On the dynamics of exploited fish populations, Chapman & Hall, London, 1957 | DOI

[6] Bocedi, G.; Heinonen, J.; Travis, J. M. J. Uncertainty and the Role of Information Acquisition in the Evolution of Context-Dependent Emigration, Am. Nat., Volume 179 (2012) no. 5, pp. 606-620 | DOI

[7] Bonte, D.; Van Dyck, H.; Bullock, J. M.; Coulon, A.; Delgado, M.; Gibbs, M.; Lehouck, V.; Matthysen, E.; Mustin, K.; Saastamoinen, M.; Schtickzelle, N.; Stevens, V. M.; Vandewoestijne, S.; Baguette, M.; Barton, K.; Benton, T. G.; Chaput-Bardy, A.; Clobert, J.; Dytham, C.; Hovestadt, T.; Meier, C. M.; Palmer, S. C. F.; Turlure, C.; Travis, J. M. J. Costs of dispersal, Biol. Rev., Volume 87 (2012) no. 2, pp. 290-312 | DOI

[8] Bowler, D. E.; Benton, T. G. Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics, Biol. Rev., Volume 80 (2005) no. 2, pp. 205-225 | DOI

[9] Brisson, J. A.; Ishikawa, A.; Miura, T. Wing development genes of the pea aphid and differential gene expression between winged and unwinged morphs: Wing development genes in the pea aphid, Insect Mol. Biol., Volume 19 (2010), pp. 63-73 | DOI

[10] Brun-Usan, M.; Rago, A.; Thies, C.; Uller, T.; Watson, R. A. Development and selective grain make plasticity 'take the lead' in adaptive evolution, BMC Ecol. Evol., Volume 21 (2021) no. 1 | DOI

[11] Chevin, L.-M.; Leung, C.; Le Rouzic, A.; Uller, T. Using phenotypic plasticity to understand the structure and evolution of the genotype–phenotype map, Genetica, Volume 150 (2022) no. 3, pp. 209-221 | DOI

[12] Clobert, J.; Galliard, J.-F. L.; Cote, J.; Meylan, S.; Massot, M. Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations, Ecol. Lett., Volume 12 (2009) no. 3, pp. 197-209 | DOI

[13] Dahirel, M.; Bertin, A.; Calcagno, V.; Duraj, C.; Fellous, S.; Groussier, G.; Lombaert, E.; Mailleret, L.; Marchand, A.; Vercken, E. Landscape connectivity alters the evolution of density-dependent dispersal during pushed range expansions, Peer Community Journal, Volume 3 (2023) | DOI

[14] Dahirel, M.; Guicharnaud, C.; Vercken, E. Individual variation in dispersal, and its sources, shape the fate of pushed vs. pulled range expansions, bioRxiv (2022) | DOI

[15] Deshpande, J. N.; Fronhofer, E. A. Genetic architecture of dispersal and local adaptation drives accelerating range expansions, Proc. Natl. Acad. Sci. U. S. A., Volume 119 (2022) no. 31 | DOI

[16] Deshpande, J. N.; Fronhofer, E. A. A gene-regulatory network model for density-dependent and sex-biased dispersal evolution during range expansions., biorxiv, 2023 | DOI

[17] Deshpande, J. N.; Fronhofer, E. A. djhelam/GRN-density-dependent-dispersal: Code associated with manuscript, Zenodo (2023) | DOI

[18] Deshpande, J. N.; Fronhofer, E. A. Supplementary Information for Deshpande and Fronhofer PCJ, Zenodo (2025) | DOI

[19] Deshpande, J. N.; Kaltz, O.; Fronhofer, E. A. Host–parasite dynamics set the ecological theatre for the evolution of state‐ and context‐dependent dispersal in hosts, Oikos, Volume 130 (2021) no. 1, pp. 121-132 | DOI

[20] Dieckmann, U.; Heino, M.; Parvinen, K. The adaptive dynamics of function-valued traits, J. Theor. Biol., Volume 241 (2006) no. 2, pp. 370-389 | DOI

[21] Draghi, J. A.; Whitlock, M. C. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation, Evolution, Volume 66 (2012) no. 9, pp. 2891-2902 | DOI

[22] Espinosa-Soto, C.; Martin, O. C.; Wagner, A. Phenotypic plasticity can facilitate adaptive evolution in gene regulatory circuits, BMC Evol. Biol., Volume 11 (2011) no. 1 | DOI

[23] Ezoe, H.; Iwasa, Y. Evolution of condition-dependent dispersal: A genetic-algorithm search for the ESS reaction norm, Population Ecology, Volume 39 (1997) no. 2, pp. 127-137 | DOI

[24] Fellous, S.; Duncan, A.; Coulon, A.; Kaltz, O. Quorum Sensing and Density-Dependent Dispersal in an Aquatic Model System, PLOS One, Volume 7 (2012) no. 11 | DOI

[25] Fronhofer, E. A.; Corenblit; Deshpande, J. N.; Govaert, L.; Huneman, P.; Viard, F.; Jarne, P.; Puijalon, S. Eco-evolution from deep time to contemporary dynamics: the role of timescales and rate modulators., Ecol. Lett., Volume 26 (2023), p. S91-S108 | DOI

[26] Fronhofer, E. A.; Gut, S.; Altermatt, F. Evolution of density-dependent movement during experimental range expansions, J. Evol. Biol., Volume 30 (2017) no. 12, pp. 2165-2176 | DOI

[27] Fronhofer, E. A.; Legrand, D.; Altermatt, F.; Ansart, A.; Blanchet, S.; Bonte, D.; Chaine, A.; Dahirel, M.; De Laender, F.; De Raedt, J.; others Bottom-up and top-down control of dispersal across major organismal groups, Nat. Ecol. Evol., Volume 2 (2018) no. 12 | DOI

[28] Fronhofer, E. A.; Kropf, T.; Altermatt, F. Density-dependent movement and the consequences of the Allee effect in the model organism Tetrahymena, J. Anim. Ecol., Volume 84 (2015) no. 3, pp. 712-722 | DOI

[29] van Gestel, J.; Weissing, F. J. Regulatory mechanisms link phenotypic plasticity to evolvability, Sci. Rep., Volume 6 (2016) no. 1 | DOI

[30] Gomulkiewicz, R.; Kirkpatrick, M. Quantitative Genetics and the Evolution of Reaction Norms, Evolution, Volume 46 (1992) no. 2 | DOI

[31] Govaert, L.; Fronhofer, E. A.; Lion, S.; Eizaguirre, C.; Bonte, D.; Egas, M.; Hendry, A. P.; De Brito Martins, A.; Melián, C. J.; Raeymaekers, J. A. M.; Ratikainen, I. I.; Saether, B.-E.; Schweitzer, J. A.; Matthews, B. Eco-evolutionary feedbacks—Theoretical models and perspectives, Funct. Ecol., Volume 33 (2019) no. 1, pp. 13-30 | DOI

[32] Gros, A.; Poethke, H. J.; Hovestadt, T. Sex-specific spatio-temporal variability in reproductive success promotes the evolution of sex-biased dispersal., Theor. Popul. Biol., Volume 76 (2009) no. 1, pp. 13-18 | DOI

[33] Gyllenberg, M.; Metz, J. A. J. On fitness in structured metapopulations, J. Math. Biol., Volume 43 (2001) no. 6, pp. 545-560 | DOI

[34] Harman, R. R.; Goddard, J.; Shivaji, R.; Cronin, J. T. Frequency of Occurrence and Population-Dynamic Consequences of Different Forms of Density-Dependent Emigration, Am. Nat., Volume 195 (2020) no. 5, pp. 851-867 | DOI

[35] Hovestadt, T.; Kubisch, A.; Poethke, H.-J. Information processing in models for density-dependent emigration: A comparison, Ecol. Model., Volume 221 (2010) no. 3, pp. 405-410 | DOI

[36] Iritani, R.; Iwasa, Y. Parasite infection drives the evolution of state-dependent dispersal of the host, Theor. Popul. Biol., Volume 92 (2014), pp. 1-13 | DOI

[37] Kun, A.; Scheuring, I. The evolution of density-dependent dispersal in a noisy spatial population model, Oikos, Volume 115 (2006) no. 2, pp. 308-320 | DOI

[38] Li, X.-Y.; Kokko, H. Sex-biased dispersal: a review of the theory, Biol. Rev., Volume 94 (2019) no. 2, pp. 721-736 | DOI

[39] Melián, C. J.; Matthews, B.; Andreazzi, C. S. d.; Rodríguez, J. P.; Harmon, L. J.; Fortuna, M. A. Deciphering the Interdependence between Ecological and Evolutionary Networks, Trends Ecol. Evol., Volume 33 (2018) no. 7, pp. 504-512 | DOI

[40] Miller, T. E. X.; Shaw, A. K.; Inouye, B. D.; Neubert, M. G. Sex-Biased Dispersal and the Speed of Two-Sex Invasions, Am. Nat., Volume 177 (2011) no. 5, pp. 549-561 | DOI

[41] Miller, T. E.; Angert, A. L.; Brown, C. D.; Lee-Yaw, J. A.; Lewis, M.; Lutscher, F.; Marculis, N. G.; Melbourne, B. A.; Shaw, A. K.; Sz\Hucs, M.; others Eco-evolutionary dynamics of range expansion, Ecology, Volume 101 (2020) no. 10 | DOI

[42] Mishra, A.; Chakraborty, P. P.; Dey, S. Dispersal evolution diminishes the negative density dependence in dispersal, Evolution, Volume 74 (2020) no. 9, pp. 2149-2157 | DOI

[43] Mullon, C. Evolved gene-regulatory networks underlying dispersal plasticity can accelerate range expansions, Peer Community in Evolutionary Biology (2025) | DOI

[44] Nichol, D.; Robertson-Tessi, M.; Anderson, A. R. A.; Jeavons, P. Model genotype–phenotype mappings and the algorithmic structure of evolution, J. R. Soc. Interface, Volume 16 (2019) no. 160 | DOI

[45] Parvinen, K.; Dieckmann, U.; Heino, M. Function-valued adaptive dynamics and the calculus of variations, Journal of Mathematical Biology, Volume 52 (2006) no. 1, pp. 1-26 | DOI

[46] Perkins, T. A.; Phillips, B. L.; Baskett, M. L.; Hastings, A. Evolution of dispersal and life history interact to drive accelerating spread of an invasive species, Ecol. Lett., Volume 16 (2013) no. 8, pp. 1079-1087 | DOI

[47] Phillips, B. L.; Brown, G. P.; Webb, J. K.; Shine, R. Invasion and the evolution of speed in toads, Nature, Volume 439 (2006) no. 7078, p. 803-803 | DOI

[48] Poethke, H. J.; Hovestadt, T. Evolution of density–and patch–size–dependent dispersal rates, Proc. R. Soc. B-Biol. Sci., Volume 269 (2002) no. 1491, pp. 637-645 | DOI

[49] Poethke, H. J.; Weisser, W. W.; Hovestadt, T. Predator‐Induced Dispersal and the Evolution of Conditional Dispersal in Correlated Environments., Am. Nat., Volume 175 (2010) no. 5, pp. 577-586 | DOI

[50] Ronce, O. How Does It Feel to Be Like a Rolling Stone? Ten Questions About Dispersal Evolution, Annu. Rev. Ecol. Evol. Syst., Volume 38 (2007) no. 1, pp. 231-253 | DOI

[51] Rünneburger, E.; Rouzic, A. L. Why and how genetic canalization evolves in gene regulatory networks, BMC Evol. Biol., Volume 16 (2016) no. 1 | DOI

[52] Saastamoinen, M.; Bocedi, G.; Cote, J.; Legrand, D.; Guillaume, F.; Wheat, C. W.; Fronhofer, E. A.; Garcia, C.; Henry, R.; Husby, A.; others Genetics of dispersal, Biol. Rev., Volume 93 (2018) no. 1, pp. 574-599 | DOI

[53] Schlichting, C. D. Hidden Reaction Norms, Cryptic Genetic Variation, and Evolvability, Ann N Y Acad Sci, Volume 1133 (2008) no. 1, pp. 187-203 | DOI

[54] Shine, R.; Brown, G. P.; Phillips, B. L. An evolutionary process that assembles phenotypes through space rather than through time, Proc. Natl. Acad. Sci. U. S. A., Volume 108 (2011) no. 14, pp. 5708-5711 | DOI

[55] Siegal, M. L.; Bergman, A. Waddington's canalization revisited: Developmental stability and evolution, Proc. Natl. Acad. Sci. U. S. A., Volume 99 (2002) no. 16, pp. 10528-10532 | DOI

[56] Spirov, A.; Holloway, D. Using evolutionary computations to understand the design and evolution of gene and cell regulatory networks, Methods, Volume 62 (2013) no. 1, pp. 39-55 | DOI

[57] Travis, J. M. J.; Dytham, C. Habitat persistence, habitat availability and the evolution of dispersal, Proc R Soc Lond B Biol Sci, Volume 266 (1999) no. 1420, pp. 723-728 | DOI

[58] Travis, J. M. J.; Mustin, K.; Benton, T. G.; Dytham, C. Accelerating invasion rates result from the evolution of density-dependent dispersal, J. Theor. Biol., Volume 259 (2009) no. 1, pp. 151-158 | DOI

[59] Wagner, A. Evolution of gene networks by gene duplications: a mathematical model and its implications on genome organization., Proc. Natl. Acad. Sci. U. S. A., Volume 91 (1994) no. 10, pp. 4387-4391 | DOI

[60] Yagound, B.; West, A. J.; Richardson, M. F.; Selechnik, D.; Shine, R.; Rollins, L. A. Brain transcriptome analysis reveals gene expression differences associated with dispersal behaviour between range‐front and range‐core populations of invasive cane toads in Australia, Mol. Ecol., Volume 31 (2022) no. 6, pp. 1700-1715 | DOI

[61] Yamamichi, M. How does genetic architecture affect eco-evolutionary dynamics? A theoretical perspective, Philos. Trans. R. Soc. B, Volume 377 (2022) no. 1855 | DOI

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