Novel pathogen introduction rapidly alters evolved movement strategies, restructuring animal societies

Animal sociality emerges from individual decisions on how to balance the costs and benefits of being sociable. Movement strategies incorporating social information — the presence and status of neighbours — can modulate spatial associations, helping animals avoid infection while benefiting from indirect information about their environment. When a novel pathogen is introduced into a population, it should increase the costs of sociality, selecting against gregariousness. Yet current thinking about novel pathogen introductions into wildlife neglects hosts’ potential evolutionary responses. We built an individual-based model that captures essential features of the repeated introduction, and subsequent transmission of an infectious pathogen among social hosts. Examining movements in a foraging context, widely shared by many species, we show how introducing a novel pathogen to a population provokes a rapid evolutionary transition to a dynamic social distancing movement strategy. This evolutionary shift triggers a disease-dominated ecological cascade of increased individual movement, decreased resource harvesting, and fewer social encounters. Pathogen-risk adapted individuals form less clustered social networks than their pathogen-risk naive ancestors, which reduces the spread of disease. The mix of post-introduction social movement strategies is influenced by the usefulness of social information and disease cost. Our work demonstrates that evolutionary adaptation to pathogen introductions and re-introductions can be very rapid, comparable to ecological timescales. Our general modelling framework shows why evolutionary dynamics should be considered in movement-disease models, and offers initial predictions for the eco-evolutionary consequences of wildlife pathogen spillover scenarios.


Introduction
and consuming food items, and to the duration that they were infected by the pathogen at the eco- 126 logical timescale. The model was implemented in R and C++ using Rcpp (Eddelbuettel 2013; R Core 127 Team 2020) and the Boost.Geometry library for spatial computations (www.boost.org); model code is at 128 github.com/pratikunterwegs/pathomove. 129 Distribution of Food Items 130 Our landscape of 60 × 60 units contains 1,800 discrete food items, which are clustered around 60 re-131 source 'kernels', for a resource density of 0.5 items per unit 2 (see SI Appendix Fig. S1 -S2). This prevents 132 synchronicity in the availability and regeneration of food items. Each available food item can be sensed 133 and harvested by foraging individuals (see below). Once harvested, another food item is regenerated at  For simplicity, we considered a population of haploid individuals with discrete, non-overlapping gen- and when the pathogen saps a percentage, rather than an absolute value, from daily intake.

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In addition to qualitative changes in social movement strategies, pathogen introduction also leads 281 to social information becoming more important to movement decisions. Prior to pathogen introduc-  is incorporated into movement strategies. Individuals using the agent avoiding strategy move more 312 than handler tracking ones ( Fig. 2A), about 85% of their lifetime (default scenario: R = 2; = 0.25). Pathogen introduction leads to the rapid replacement, within 25 generations, of agent tracking with 'handler tracking' (preference for successful foragers; 3,000 < < 3,025). Within 250 generations, 'agent avoidance' (avoidance of both successful and unsuccessful foragers; > 3,250) also becomes common, stably co-existing with the handler tracking strategy in an eco-evolutionary equilibrium. (B) After pathogen introduction ( > 3,000), the importance of social cues (the presence of other individuals; the sum of the absolute, normalised preferences , ) increases substantially on average (grey points). Additionally, there is significant variation in the importance of social cues to individuals (shaded regions), which is not captured by the mean or standard error. At G = 4,500, for example, social information comprises ≈ 10% of some individuals' movement strategies, but some individuals have evolved a stronger weight for social cues (> 20%). The rapid change in social movement strategies following pathogen introduction has cascading effects on ecological outcomes. Individuals, which have evolved strong aversions to at least some kinds of foragers (depending on their strategy), (C) move more on average, (D) have only 25% of the pre-pathogen average intake, and (E) have 100-fold fewer associations with other individuals. All panels show data averaged over 10 replicates, but shaded region in panel B shows only a single replicate for clarity. tively (Fig. 2B). All other strategies, especially the agent tracking strategy common in pre-introduction 318 populations, are barely able to translate increased movement into fewer associations (Fig. 2A). These 319 strategies have a wide range of infection rates (Fig. 2B), potentially because they are very rare -these 320 likely represent mutants that do not give rise to persistent lineages.

Figure 2: Social movement strategies trade movement for associations through dynamic social distancing, leading to differences in infection rates.
In post-introduction populations at ecoevolutionary equilibrium (G > 3,500), (A) both agent avoiding and handler tracking individuals can reduce encounters with other individuals by moving to avoid other foragers (dynamic social distancing). Handler tracking individuals have many more encounters than agent avoiding individuals, but surprisingly, are better able to reduce encounters through increased movement. Individuals using other strategies (mostly agent tracking) have a wider range of movement distances, but cannot efficiently avoid other foragers by moving more. (B) Avoiding all other foragers leads to marginally lower infection rates than tracking successful foragers (and avoiding unsuccessful ones; handler tracking). Surprisingly, rare pre-introduction strategies such as following any nearby individuals (agent tracking) may also have low infection rates, potentially due to their rarity. Panel A shows linear model fits with a log scale Y-axis; panel B shows infection rates; all data represent generation-and replicate-specific means (G > 3,500; R = 2, = 0.25).

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Following pathogen introduction, the mixture of individual-level movement strategies elicits a substan-323 tial re-organisation of emergent spatial and social structure at the population level. Pre-introduction 324 populations are strongly clustered in space (Fig. 3A), due to movement strategies that favour following 325 most other foragers. This spatial proximity means that most individuals encounter each other at least 326 once, leading to numerous unique partners (the 'degree') for each forager (Fig. 3 inset 1: blue). In con-327 13 trast, the spread-out networks in pathogen-risk adapted populations suggest that most foragers move substantially from their initial locations over their lifetime, associating only ephemerally with foragers 329 from all over the landscape (Fig. 3B). This reflects movement strategies which lead to near-perpetual counter fewer than 10% of the population over their lifetime (Fig. 3 inset 1: red).

Usefulness of Social Information and Infection Cost Influence Evolution of 353
Social Movement Strategies 354 We further explored the effect of two ecological parameters, landscape productivity ( ∈ 1, 2, 5) and 355 infection cost per timestep ( ∈ 0.1, 0.25, 0.5) on simulation outcomes. Before pathogen introduction, 356 landscape productivity alone determines the value of social information, and thus which social move-357 ment strategies evolve (Fig. 4). On low-productivity landscapes (R = 1), social information is valuable  Pre-introduction (G = 3,000; dashed line) populations contain a mix of individuals that either track all foragers (agent tracking), or only successful foragers (handler tracking). Handler tracking is more common on low-productivity landscapes (R = 1), where social information is more useful to find patchily distributed resources. After pathogen introduction, handler tracking rapidly becomes the most common strategy when the apparent usefulness of social information is greater than the cost of infection. This occurs both when productivity is low (R = 1) and infection costs are low ( = 0.1), but also when productivity is high (R = 5) with intermediate infection costs ( = 0.25). When the cost of infection outweighs the apparent usefulness of social information, the agent avoidance (avoiding both successful and unsuccessful foragers) emerges and rapidly becomes a common strategy ( = 0.5; = 0.25, R = 1). In scenarios of high landscape productivity combined with low infection costs (e.g. R = 5, = 0.1), the agent tracking strategy persists in a large proportion after pathogen introduction, as these individuals can balance disease costs with intake alone. All panels show mean frequencies over 10 replicate simulations in 100 generation bins; frequencies are stacked. Grey areas show the relatively uncommon 'non-handler' tracking strategy. 16 landscapes ( ∈ 2, 5), social information is less valuable as individuals can directly detect food items 360 more often; here, the agent tracking strategy is most common. Across parameter combinations, the in-361 troduction of the infectious pathogen leads to a rapid evolutionary shift in social movement strategies.

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The benefits of social information, and infection cost jointly determine how pathogen introduction al-363 ters the mix of social movement strategies, but populations generally shift away from indiscriminate 364 agent tracking, as that strategy is associated with higher infection risk (see Fig. 3A).

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When the benefit of social information is equivalent to the cost of infection, the handler tracking