Enhancing the ecological realism of evolutionary mismatch theory

Pollack, Lea; Munson, Amelia; Savoca, Matthew S.; Trimmer, Pete C.; Ehlman, Sean M.; Gil, Michael A.; Sih, Andrew

doi:10.1016/j.tree.2021.10.011

Cited by 14 publications

(9 citation statements)

References 122 publications

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“…Correctly identifying and evaluating the social salience of available light levels in the environment poses a challenge. Regardless of modality, filtering signals from noise is a sensory and perceptual task [50] that has large fitness consequences (e.g. [51,52]).…”

Section: Discussionmentioning

confidence: 99%

Collective synchrony of mating signals modulated by ecological cues and social signals in bioluminescent sea fireflies

Hensley,

Rivers,

Gerrish

et al. 2023

Proc. R. Soc. B.

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Individuals often employ simple rules that can emergently synchronize behaviour. Some collective behaviours are intuitively beneficial, but others like mate signalling in leks occur across taxa despite theoretical individual costs. Whether disparate instances of synchronous signalling are similarly organized is unknown, largely due to challenges observing many individuals simultaneously. Recording field collectives and ex situ playback experiments, we describe principles of synchronous bioluminescent signals produced by marine ostracods (Crustacea; Luxorina) that seem behaviorally convergent with terrestrial fireflies, and with whom they last shared a common ancestor over 500 Mya. Like synchronous fireflies, groups of signalling males use visual cues (intensity and duration of light) to decide when to signal. Individual ostracods also modulate their signal based on the distance to nearest neighbours. During peak darkness, luminescent ‘waves’ of synchronous displays emerge and ripple across the sea floor approximately every 60 s, but such periodicity decays within and between nights after the full moon. Our data reveal these bioluminescent aggregations are sensitive to both ecological and social light sources. Because the function of collective signals is difficult to dissect, evolutionary convergence, like in the synchronous visual displays of diverse arthropods, provides natural replicates to understand the generalities that produce emergent group behaviour.

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Section: Discussionmentioning

confidence: 99%

Collective synchrony of mating signals modulated by ecological cues and social signals in bioluminescent sea fireflies

Hensley,

Rivers,

Gerrish

et al. 2023

Proc. R. Soc. B.

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“…Signal detection theory (SDT) provides predictions on factors affecting the cue threshold, and thus the relative likelihood that animals will respond to fire cues. SDT has been used to explain variation in mate or food choice (Holen & Sherratt, 2021; Pearse et al, 2013), evolutionary traps involving habitat choice (Pollack et al, 2021; Robertson et al, 2013) and the decision to ignore versus respond to predators or other potential threats (Ehlman et al, 2019; Trimmer, Ehlman, McNamara, et al, 2017; Trimmer, Ehlman, & Sih, 2017). For simplicity, SDT typically assumes that animals choose between two actions (e.g.…”

Section: Proposed Framework: the Parallels Between Fear Of Fire And F...mentioning

confidence: 99%

“…In these situations, animals might still attempt to disperse because it used to be adaptive even if it is now futile. The cues that trigger dispersal are then an evolutionary trap (Pollack et al, 2021;Robertson et al, 2013), where previously adaptive cue-response systems now produce a maladaptive response.…”

Section: Box 3 Previously Adaptive Dispersal a Trap In The Anthropocene?mentioning

confidence: 99%

“…Similarly, wallabies ( Wallabia bicolor ) that are quite mobile, may actually fare better if they seek refuge on nearby, rocky outcrops or riverine refugia, rather than fleeing (Garvey et al, 2010; Recher et al, 1975; Thornett et al, 2016). For animals that dispersed when they should have sought local refuge, the cues that triggered dispersal could be considered a form of evolutionary trap (Pollack et al, 2021; Robertson et al, 2013; Sih et al, 2020) where previously adaptive cue‐response systems now result in maladaptive behaviours (Box 3).…”

Section: Proposed Framework: the Parallels Between Fear Of Fire And F...mentioning

confidence: 99%

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Integrating sensory ecology and predator‐prey theory to understand animal responses to fire

et al. 2023

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Fire regimes are changing dramatically worldwide due to climate change, habitat conversion, and the suppression of Indigenous landscape management. Although there has been extensive work on plant responses to fire, including their adaptations to withstand fire and long-term effects of fire on plant communities, less is known about animal responses to fire. Ecologists lack a conceptual framework for understanding behavioural responses to fire, which can hinder wildlife conservation and management. Here, we integrate cue-response sensory ecology and predatorprey theory to predict and explain variation in if, when and how animals react to approaching fire. Inspired by the literature on prey responses to predation risk, this framework considers both fire-naïve and fire-adapted animals and follows three key steps: vigilance, cue detection and response. We draw from theory on vigilance tradeoffs, signal detection, speed-accuracy tradeoffs, fear generalization, neophobia and adaptive dispersal. We discuss how evolutionary history with fire, but also other selective pressures, such as predation risk, should influence animal behavioural responses to fire. We conclude by providing guidance for empiricists and outlining potential conservation applications.

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“…Environmental changes exacerbate the evolutionary mismatch among microbial and eukaryotic interaction partners, characterized by distinct generation times, mutation rates and populations sizes (61). This creates fertile ground for the emergence of marine diseases, often facilitated by rapid shifts in microbial dynamics across the mutualismparasitism continuum (62).…”

Section: Introductionmentioning

confidence: 99%

Parent-specific transgenerational immune priming enhances offspring defense – unless heat-stress negates it all

Schneider,

Dubin,

Marten

et al. 2024

Preprint

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Trans-generational immune priming (TGIP) adjusts offspring immune responses based on parental immunological experiences - a form of trans-generational plasticity predicted to be adaptive when parent-offspring environmental conditions match. In contrast, mis-matches between environmental conditions negate those advantages, rendering TGIP costly when mismatched immunological offspring phenotypes are induced. Particularly maternal TGIP was thought to shape offspring immunological preparedness: mothers' eggs contain more substance than sperm and, in viviparous species, pregnancy provides additional avenues for immune priming of developing offspring. The syngnathids' (pipefishes and seahorses) unique male pregnancy provides an unusual perspective to the ecological relevance of TGIP in a system where egg production and pregnancy occur in different sexes. We simulated parental bacteria exposure in broad nosed pipefish, Syngnathus typhle, through vaccinations with heat-killed Vibrio aestuarianus before mating the fish to each other or control individuals. Resulting offspring were raised, and some exposed to V. aestuarianus, in a control or heat-stress environment, after which transcriptome and microbiome compositions were investigated. Transcriptomic TGIP effects were only observed in Vibrio-exposed offspring at control temperatures, arguing for low costs of TGIP in non-matching environments. Transcriptomic phenotypes elicited by maternal and paternal TGIP had only limited overlap and were not additive. Both transcriptomic responses were significantly associated to immune functions, and specifically the paternal response to the innate immune branch. TGIP of both parents reduced the relative abundance of the experimental Vibrio in exposed offspring, showcasing its ecological effectiveness. Despite its significance in matching biotic environments, no TGIP-associated phenotypes were observed for heat-treated offspring. Heat-spikes caused by climate change thus threaten TGIP benefits, potentially increasing susceptibility to emerging marine diseases. This highlights the urgent need to understand how animals will cope with climate-induced changes in microbial assemblages by illustrating the importance - and limits - of TGIP in mitigating the impacts of environmental stressors on offspring vulnerability.

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Enhancing the ecological realism of evolutionary mismatch theory

Cited by 14 publications

References 122 publications

Collective synchrony of mating signals modulated by ecological cues and social signals in bioluminescent sea fireflies

Collective synchrony of mating signals modulated by ecological cues and social signals in bioluminescent sea fireflies

Integrating sensory ecology and predator‐prey theory to understand animal responses to fire

Parent-specific transgenerational immune priming enhances offspring defense – unless heat-stress negates it all

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