Resource Competition Shapes Biological Rhythms and Promotes Temporal Niche
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bioRxiv preprint doi: https://doi.org/10.1101/2020.04.22.055160; this version posted April 22, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 2 3 Resource competition shapes biological rhythms and promotes temporal niche 4 differentiation in a community simulation 5 6 Resource competition, biological rhythms, and temporal niches 7 8 Vance Difan Gao1,2*, Sara Morley-Fletcher1,4, Stefania Maccari1,3,4, Martha Hotz Vitaterna2, Fred W. Turek2 9 10 1UMR 8576 Unité de Glycobiologie Structurale et Fonctionnelle, Campus Cité Scientifique, CNRS, University of 11 Lille, Lille, France 12 2 Center for Sleep and Circadian Biology, Northwestern University, Evanston, IL, United States of America 13 3Department of Medico-Surgical Sciences and Biotechnologies, University Sapienza of Rome, Rome, Italy 14 4International Associated Laboratory (LIA) “Perinatal Stress and Neurodegenerative Diseases”: University of Lille, 15 Lille, France; CNRS-UMR 8576, Lille, France; Sapienza University of Rome, Rome, Italy; IRCCS Neuromed, Pozzilli, 16 Italy 17 18 19 * Corresponding author 20 E-mail: [email protected] 21 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.22.055160; this version posted April 22, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 22 Abstract 23 Competition for resources often contributes strongly to defining an organism’s ecological niche. Biological 24 rhythms are important adaptations to the temporal dimension of niches, but the role of other organisms in 25 determining such temporal niches have not been much studied, and the role specifically of competition even 26 less so. We investigate how interspecific and intraspecific competition for resources shapes an organism’s 27 activity rhythms. For this, communities of one or two species in an environment with limited resource input 28 were simulated. We demonstrate that when organisms are arrhythmic, one species will always be competitively 29 excluded from the environment, but the existence of activity rhythms allows niche differentiation and indefinite 30 coexistence of the two species. Two species which are initially active at the same phase will differentiate their 31 phase angle of entrainment over time to avoid each other. When only one species is present in an environment, 32 competition within individuals of the species strongly selects for niche expansion through arrhythmicity, but the 33 addition of an interspecific competitor facilitates evolution of increased rhythmic amplitude when combined 34 with additional adaptations for temporal specialization. Finally, if individuals preferentially mate with others 35 who are active at similar times of day, then disruptive selection by intraspecific competition can split one 36 population into two reproductively isolated groups. In summary, these simulations suggest that biological 37 rhythms are an effective method to temporally differentiate ecological niches, and that competition is an 38 important ecological pressure promoting the evolution of rhythms and sleep. 39 40 Author summary 41 Why do we sleep? We are interested in the ecological factors which promote the evolution of biological 42 rhythms like the sleep-wake cycle, focusing especially on competition. When animals compete with each other 43 for resources, they often evolve to avoid each other by specializing to use different resources or separating their 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.22.055160; this version posted April 22, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 44 activity in other ways. To test hypotheses about how competition shapes rest-activity rhythms, we performed 45 computer simulations of a community of animals who move, reproduce, and compete for resources. We show 46 that biological rhythms let two species divide time so that one species is active while its competitor is resting, 47 thus avoiding depleting shared resources. When a species has no competitors in the simulation, competition 48 between members of the same species cause population and individual rhythms to decrease, since resource 49 availability is low when everybody is active at the same time. However, having competitors allows strong 50 rhythms to evolve from originally arrhythmic organisms. Competition can even cause a single population to split 51 into two species which are separated in time. In summary, these results suggest that competition is a strong 52 factor promoting rest-activity rhythms. 53 54 Introduction 55 An ecological niche is the particular “space” a species occupies in an ecosystem, comprising a diversity of 56 concepts including the physical environment where it lives, the resources it uses, its interactions with other 57 species, and the adaptations it has evolved to exploit the niche. Both theory and evidence indicate that 58 competition is a major factor which determines species’ niches [1,2]. Competitors for a resource generally will 59 adjust to avoid each other, differentiating their niches by adapting to utilize different types of resources, thus 60 avoiding the depletion of shared resources (exploitative competition) [3] as well as costly acts of aggression and 61 territorial exclusion (interference competition) [4]. 62 Time is one dimension which defines a niche. Most species live in environments dominated by a day-night 63 cycle and a seasonal cycle, though other cycles such as tides can also strongly define an ecosystem [5]. A 64 temporal niche is defined by both abiotic elements such as light intensity and temperature [6,7], as well the as 65 by predictable temporal patterns of other organisms [8]. Adaptions for a specific temporal niche include for 66 example specializations in vision, coat color, temperature regulation, and importantly, biological rhythms, i.e. 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.22.055160; this version posted April 22, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 67 physiological and behavioral traits which cycle regularly according to an internal biological clock . In this article, 68 we consider activity rhythms through the lens of ecological niche theory, viewing them as a way partition niches 69 among competitors and examining how competition shapes the expression of these biological clocks. Time can 70 be thus viewed as a sort of resource or space which is partitioned by organisms in response to competition [9], 71 both interspecific (between different species) and intraspecific (between members of the same species) [10]. 72 While some work has examined predation’s effect on animals’ activity rhythms [11–13], the role of competition 73 has been less examined. 74 A variety of field studies have observed evidence of temporal partitioning between putative competitors. 75 For example, a community of three sympatric species of insectivorous bats were observed to have activity 76 profiles which are displaced from each other, suggesting that they avoid each other [14]. While Argentinian 77 pampas foxes are normally nocturnal, they show a modified half-nocturnal half-diurnal profile in a region where 78 they overlap with crab-eating foxes [15]. Other examples of apparent temporal partitioning have been seen at 79 watering holes [16,17], in desert gerbils [18], carabid beetles [19], and large African carnivores [20]. Stronger 80 evidence comes from semi-natural manipulation experiments. Common spiny mice are nocturnal and golden 81 spiny mice are diurnal in areas where the two species coexist, but when the common spiny mice are 82 experimentally removed, the originally diurnal golden spiny mice shift into nocturnality, suggesting that this 83 species was pushed into diurnality by the competing species [9]. It should be recognized that these examples all 84 occur at the behavioral and ecological time scale, i.e. they are “temporary” displacements from the species’ 85 genetically determined preferred activity time. Although certain pairs of taxa are suggestive of evolutionary- 86 level temporal partitioning—nocturnal owls and diurnal hawks, for instance, or the hypothesized nocturnal 87 origin of mammals [21]—the role of competition in causing these evolutionary divergences is near impossible to 88 establish conclusively. Nonetheless, it is probable that temporal shifts at the behavioral/ecological level cause 89 selection for alleles suited for the new time period, eventually translating into long-term changes at the 90 genetic/evolutionary level. 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.22.055160; this version posted April 22, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 91 In this work, we explore ways which competition in ecological niche theory can be applied to biological 92 rhythms, using simulation of a community of two species who compete for limited resources in an environment. 93 We first demonstrate that circadian rhythms are a form of niche differentiation which allows two species to 94 stably coexist without competitive exclusion, and that two rhythmic species will quickly differentiate their 95 circadian phases to avoid competition. We show that arrhythmicity is preferred when there is no interspecific 96 competitor present, but the presence of interspecific competition greatly facilitates the development of strong 97 activity rhythms.