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Biology subjects

Fisher, D. N.

Publications and source records attributed to Fisher, D. N..

At least 19 recordsLinked to original sources

Analgesic preference and injury behaviour in Blaptica dubia

Insects are increasingly recognised as behaviourally complex animals, yet whether they experience pain as an affective state beyond nociception remains unresolved. Voluntary ingestion of analgesics by injured individuals has been proposed as a key but largely untested criterion for evaluating insect pain. This study tested whether wing-clipped Blaptica dubia preferentially consumed an ibuprofen-sucrose solution over sucrose alone, and whether injury altered the duration of abnormal behaviour.. Adult males were assigned to injured or sham-handled groups and completed 30-minute two-choice assays.. Choice between the analgesic, sucrose-only and neutral zones were recorded, as well as recording the duration of a range of abnormal behaviours. The experiment was repeated with vanilla scent added to both solutions as a masking agent.. Injured cockroaches did not show greater analgesic preference in either condition. Instead, the vanilla condition markedly reduced preference for the analgesic.. Injury strongly increased the duration of abnormal behaviours, with increases in the duration of body flexion, lateral swaying, and wing fluttering, while wing-directed grooming was rare but showed a tendency for increases when injured. These findings provide no evidence that injured B. dubia actively seek an orally delivered analgesic under the conditions tested. However, injury produced clear and sustained behavioural disruption consistent with an internally driven aversive or discomfort-related state, highlighting both the methodological challenges of adapting voluntary analgesic assays to insects and the welfare relevance of injury in B. dubia.

animal behavior and cognition↗

Pessimistic and optimistic cognitive biases in cockroaches

Understanding the subjective experience of animals is key for how we manage them and for mapping the evolution of cognitive complexity. Emotional and affective are fundamental to these goals as their presence indicates the potential for subjective experiences and suffering. However, until recently the potential for affective states in invertebrates has been underappreciated, especially for positive affective states where research is limited to a single order. Here, we adapt cognitive bias tests to examine both negative (pessimistic) and positive (optimistic) bias in cockroaches (Blaptica dubia) in order to expand the taxonomic reach of affective state research and to provide a rare test for positive affective states in an invertebrate. We trained cockroaches to associate two different odours with either positive or negative reinforcement and then assessed their reactions to ambiguous stimuli (a range of mixtures of the trained odours). We found that cockroaches exposed to light were more pessimistic (negative affective state) than controls, while those exposed to the scent of opposite sex conspecifics were marginally more optimistic (positive affective state) than controls. We therefore demonstrate the potential for affective states in cockroaches and for positive affective states in invertebrates more widely, indicating a hereto unexpected level of cognitive complexity.

animal behavior and cognition↗

Motivational trade-offs in a cockroach: impact of conditions, injury, and development

The ability to flexibly trade off access between competing or antagonistic stimuli ("motivational trade-offs") is a key criterion for assessing whether animals can feel pain. However, in some commonly farmed, exterminated, and studied insect orders such as Blattodea (cockroaches and termites), the ability to make motivational trade-offs is unconfirmed, which makes it difficult to assess their welfare needs. Here we gave cockroaches (Blaptica dubia) a choice between access to shelter or to nutrition across a series of linked experiments to assess whether they are capable of motivational trade-offs and if they are flexibly adjusted due to external conditions and/or injury and develop across ontogeny. We found cockroaches avoided a food reward when it was exposed to light (a behavioural trade-off), but they did not adjust their preference flexibly in response to lighting intensity or increased hunger level (no motivational trade-off). We did find that injury reduces willingness to accept light exposure when accessing nutrition, which is consistent with the idea of the sensation of pain reducing risk-taking behaviour. Finally, we showed that juvenile cockroaches match adults in not making a motivational trade-off. All together our results provide much-needed evidence for criteria of whether insects feel pain and suggest upper limits to cognitive complexity and flexibility in Blattodea. These findings can be integrated with other neurological and behavioural measures to help us judge how we treat insects and other invertebrates in our care.

animal behavior and cognition↗

Multilevel-consistency of social behaviour in a cockroach

Group-living animals may show consistency in both individual behaviour and group-level behaviour. Further, while individuals show consistent differences in their responses to environmental change (plasticity), it is less clear if groups differ in plasticity. Here we exposed groups of cockroaches (Blaptica dubia) to three humidities and quantified their social networks. We repeated our design across multiple groups with individuals reassigned to different groups and used machine vision analysis of images to extract 152,800 records of associations across 16 different groups. 116 unique individuals contributed >4,500 individual social network measures and 192 measures of entire networks. Lower humidity led to individuals that had slightly better connectedness to the whole network, but otherwise did not impact individual or group-level phenotypes. Individuals showed some consistency in mean behaviours (12-39%) but scant consistency in plasticity (0-9%). In contrast, groups showed less consistency in mean behaviours than individuals (0-26%) but showed relatively higher among-group differences in plasticity compared to individuals (0-22%). Patterns of group-level variance in individual traits matched patterns of variance in characteristics of entire networks, suggesting these two approaches for quantifying group phenotypes are compatible. While consistency in individual mean behaviour is the norm across taxa, consistency in group-level plasticity is less well understood and may be an emergent phenomenon of collective dynamics that deserves further investigation. Using automated marker recognition techniques such as machine vision allows us to collect the large datasets necessary to simultaneously test hypotheses at the individual and group level and so can be more widely adopted.

animal behavior and cognition↗

Examining the fitness benefits of social plasticity to prey availability in bottlenose dolphins

A key explanation for phenotypic plasticity is that changing behaviour to match conditions increases fitness. Affiliative social associations with conspecifics can be important for coping with challenging conditions, and therefore plasticity in social behaviour in response to environment variation may bring fitness benefits. Here we leverage a dataset of 711 observations of 62 female bottlenose dolphins (Tursiops truncatus) over 35 years to estimate the plastic responses in social behaviour to salmon (Salmo salar) abundance and determine if either this plasticity or their mean social behaviour is associated with lifetime calving success. We found no evidence that mean social behaviour or plasticity in response to salmon abundance were associated with this component of fitness. Female dolphins did not seem to adjust their social behaviour to buffer low, or take advantage of high, salmon abundance and this prey variability was not associated with female reproductive success. Limitations in the data and follow-up simulations suggest that these null relationships, especially for plasticity, may be due to a lack of power, highlighting the difficulty of estimating these covariances even in long term studies with large datasets.

animal behavior and cognition↗

Measuring the effect of RFID and Marker Recognition tags on cockroach behaviour using AI aided tracking

RFID technology and marker recognition algorithms can offer an efficient and non-intrusive means of tracking animal positions. As such, they have become important tools for invertebrate behavioural research. Both approaches require fixing a tag or marker to the study organism, and so it is useful to quantify the effects such procedures have on behaviour before proceeding with further research. However, frequently studies do not report doing such tests. Here, we demonstrate a time-efficient and accessible method for quantifying the impact of tagging on individual movement using open-source automated video tracking software. We tested the effect of RFID tags and tags suitable for marker recognition algorithms on the movement of Argentinian wood roaches (Blapicta dubia) by filming tagged and untagged roaches in laboratory conditions. We employed DeepLabCut on the resultant videos to track cockroach movement and extract measures of behavioural traits. We found no statistically significant differences between RFID tagged and untagged groups in average speed over the trial period, the number of unique zones explored, and the number of discrete walks. However, groups that were tagged with labels for marker recognition had significantly higher values for all three metrics. We therefore support the use of RFID tags to monitor the behaviour of B. dubia but note that the effect of using labels suitable for label recognition to identify individuals should be taken into consideration when measuring B.dubia behaviour. We hope that this study can provide an accessible and viable roadmap for further work investigating the effects of tagging on insect behaviour.

animal behavior and cognition↗

Exploring changes in social spider DNA methylation profiles when succumbing to infection in CpG, CHG, and CHH contexts

Living at high density and with low genetic diversity are factors that should both increase the susceptibility of organisms to disease. Therefore, group living organisms, especially those that are inbred, should be especially vulnerable to infection and therefore have particular strategies to cope with infection. Phenotypic plasticity, underpinned by epigenetic changes, could allow group living organisms to rapidly respond to infection challenges. To explore the potential role of epigenetic modifications in the immune response to a group-living species with low genetic diversity, we compared the genome-wide DNA methylation profiles of five colonies of social spiders (Stegodyphus dumicola) in their natural habitat in Namibia at the point just before they succumbed to infection to a point at least six months previously where they were presumably healthier. We found increases in genome- and chromosome-wide methylation levels in the CpG, CHG, and CHH contexts, although the genome-wide changes were not clearly different from zero. These changes were most prominent in the CHG context, especially at a narrow region of chromosome 13, hinting at an as-of-yet unsuspected role of this DNA methylation context in phenotypic plasticity. However, there were few clear patterns of differential methylation at the base level, and genes with a known immune function in spiders had mean methylation changes close to zero. Our results suggest that DNA methylation may change with infection at large genomic scales, but that this type of epigenetic change is not necessarily integral to the immune response of social spiders.

genomics↗

Indirect genetic effects increase the heritable variation available to selection and are largest for behaviours: a meta-analysis

The evolutionary potential of traits is governed by the amount of heritable variation available to selection. While this is typically quantified based on genetic variation in a focal individual for its own traits (direct genetic effects, DGEs), when social interactions occur, genetic variation in interacting partners can influence a focal individuals traits (indirect genetic effects, IGEs). Theory and studies on domesticated species have suggested IGEs can greatly impact evolutionary trajectories, but whether this is true more broadly remains unclear. Here we perform a systematic review and meta-analysis to quantify the amount of trait variance explained by IGEs and the contribution of IGEs to predictions of adaptive potential. We identified 180 effect sizes from 47 studies across 21 species and found that, on average, IGEs of a single social partner account for a small but statistically significant amount of phenotypic variation (0.03). As IGEs affect the trait values of each interacting group member and due to a typically positive - although statistically nonsignificant - correlation with DGEs (rDGE-IGE = 0.26), IGEs ultimately increase trait heritability substantially from 0.27 (narrow-sense heritability) to 0.45 (total heritable variance). This 66% average increase in heritability suggests IGEs can increase the amount of genetic variation available to selection. Furthermore, whilst showing considerable variation across studies, IGEs were most prominent for behaviours, and to a lesser extent for reproduction and survival, in contrast to morphological, metabolic, physiological, and development traits. Our meta-analysis therefore shows that IGEs tend to enhance the evolutionary potential of traits, especially for those tightly related to interactions with other individuals such as behaviour and reproduction. Lay SummaryPredicting evolutionary change is important for breeding better livestock and crops, for understanding how biodiversity arises and how populations respond to environmental change. Normally, these predictions are based on how the genetic variants in an organism influence its own traits (characteristics). However, when organisms socially interact, for instance by fighting or cooperating, then the genes in one individual can influence the traits of others, therefore affecting the potential for evolutionary change. We compared 47 studies across 21 animal species and found that the effect of the genes of a single social partner is small but statistically significant, while the total contribution of social genetic effects to evolutionary potential is large. These effects are particularly important for the evolution of animals behaviours and reproductive traits, but less so for other traits such as body size and physiology. We also found that, because an individual can interact with many others and influence them all, social interactions can substantially increase the potential for a population to evolve from generation to generation. Our results show how social interactions can potentially alter the evolution of those traits known to respond to social interactions in comparison to standard expectations.

evolutionary biology↗

Cockroach social network position does not influence dispersal tendency

In group-living organisms, we might expect relationships between social position and exploration, such as if certain patterns of social associations encourage exploration or if certain personality types both link different groups and are more likely to explore their environment. However, directly testing these ideas is challenging as exploration can be hard to track in the field and is a difficult trait to measure in the laboratory. Furthermore, invertebrate exploration is less commonly quantified as their small size makes them hard to track. Here we quantified social networks in multiple groups of the gregarious cockroach Blaptica dubia in the laboratory and related three measures of social network position (representing overall sociability, connectedness in local cliques, and connectedness to the wider network) to measures of exploration either assayed alone or as part of a group. We found none of the social network measures related to either of the measures of exploration, which were themselves not correlated. We also found that sociability and connectedness to the wider network were positively correlated, suggesting a single axis of variation in centrality within a group. We found no effects of mass or sex, but there were differences between the two blocks our experiments were performed in, suggesting some effect of observer variability. Overall, our results suggest that exploration is not linked to social behaviour in this species, that cockroaches differ in the social behaviour along a syndrome integrating sociability and the tendency to move between groups, and that study replication should be encouraged so we can be confident identified trends are robust.

animal behavior and cognition↗

Dolphin social phenotypes typically show individual variation in response to environmental change alongside population-level stability

Social behaviours can allow individuals to flexibly respond to environmental change, potentially buffering adverse effects. However, individuals may respond differently to the same environmental stimulus, complicating predictions for population-level response to environmental change. Here we show that bottlenose dolphins (Tursiops truncatus) alter their social behaviour at yearly and monthly scales in response to a proxy for food availability (salmon abundance) but do not respond to variation in a proxy for climate (the North Atlantic Oscillation index). There was also individual variation in plasticity for gregariousness and connectedness to distant parts of the social network, although these traits showed limited repeatability. In contrast, individuals showed consistent differences in clustering with their immediate social environment at the yearly scale but no individual variation in plasticity for this trait at either time scale. These results indicate that social behaviour in free-ranging cetaceans can be highly resource dependent with individuals increasing their connectedness over short timescales but possibly reducing their wider range of connection at longer timescales. Some social traits showed more individual variation in plasticity or mean behaviour than others, highlighting how predictions for the responses of populations to environmental variation must consider the type of individual variation present in the population.

ecology↗

Direct and indirect phenotypic effects on sociability indicate potential to evolve

The decision to leave or join a group is important as group size influences many aspects of organisms lives and their fitness. This tendency to socialise with others, sociability, should be influenced by genes carried by focal individuals (direct genetic effects) and by genes in partner individuals (indirect genetic effects), indicating the traits evolution could be slower or faster than expected. However, estimating these genetic parameters is difficult. Here, in a laboratory population of the cockroach Blaptica dubia, I estimate phenotypic parameters for sociability: repeatability (R) and repeatable influence (RI), that indicate whether direct and indirect genetic effects respectively are likely. I also estimate the interaction coefficient ({Psi}), which quantifies how strongly a partners trait influences the phenotype of the focal individual and is key in models for the evolution of interacting phenotypes. Focal individuals were somewhat repeatable for sociability across a three-week period (R = 0.083), and partners also had marginally consistent effects on focal sociability (RI = 0.055). The interaction coefficient was non-zero, although in opposite sign for the sexes; males preferred to associate with larger individuals ({Psi}male = -0.129) while females preferred to associate with smaller individuals ({Psi}female = 0.068). Individual sociability was consistent between dyadic trials and in social networks of groups. These results provide phenotypic evidence that direct and indirect genetic effects have limited influence on sociability, with perhaps most evolutionary potential stemming from heritable effects of the body mass of partners. Sex-specific interaction coefficients may produce sexual conflict and the evolution of sexual dimorphism in social behaviour.

evolutionary biology↗

Social selection and the evolution of maladaptation

Evolution by natural selection is often viewed as a process that inevitably leads to adaptation, or an increase in population fitness over time. However, maladaptation, an evolved decrease in fitness, may also occur in response to natural selection under some conditions. Social selection, which arises from the effects of social partners on fitness, has been identified as a potential cause of maladaptation, but we lack a general rule identifying when social selection should lead to a decrease in population mean fitness. Here we use a quantitative genetic model to develop such a rule. We show that maladaptation is most likely to occur when social selection is strong relative to nonsocial selection and acts in an opposing direction. In this scenario, the evolution of traits that impose fitness costs on others may outweigh evolved gains in fitness for the individual, leading to a net decrease in population mean fitness. Further, we find that maladaptation may also sometimes occur when phenotypes of interacting individuals negatively covary. We outline the biological situations where maladaptation in response to social selection can be expected, provide both quantitative genetic and phenotypic versions of our derived result, and suggest what empirical work would be needed to test it. We also consider the effect of social selection on inclusive fitness and support previous work showing that inclusive fitness cannot suffer an evolutionary decrease. Taken together, our results show that social selection may decrease population mean fitness when it opposes individual-level selection, even as inclusive fitness increases. Subject areaQuantitative genetics and Mendelian inheritance

evolutionary biology↗

Social selection is density dependent but makes little contribution to total selection in New Zealand giraffe weevils

Social selection occurs when traits of interaction partners influence an individuals fitness and can fundamentally alter total selection strength. Unlike for direct selection, however, we have little idea of what factors influence the strength of social selection. Further, social selection only contributes to overall selection when there is phenotypic assortment, but simultaneous estimates of social selection and phenotypic assortment are rare. Here we estimated social selection on body size in a wild population of New Zealand giraffe weevils (Lasiorhynchus barbicornis). We did this in a range of contexts and measured phenotypic assortment for both sexes. Social selection was mostly absent and not affected by sex ratio or the body size of the focal individual. However, at high densities selection was negative for both sexes, consistent with competitive interactions based on size for access to mates. Phenotypic assortment was also density dependent, flipping from positive at low densities to negative at high densities. However, it was always close to zero, indicating negative social selection at high densities will not greatly impede the evolution of larger body sizes. Despite its predicted importance, social selection may only influence evolutionary change in specific contexts, leaving direct selection as the dominant driver of evolutionary change.

evolutionary biology↗

Behavioral and physiological evidence that increasing group size ameliorates the impacts of social disturbance

Intra-group social stability is important for the long-term productivity and health of social organisms. We evaluated the effect of group size on group stability in the face of repeated social perturbations using a cooperatively breeding fish, Neolamprologus pulcher. In a laboratory study, we compared both the social and physiological responses of individuals from small versus large groups to the repeated removal and replacement of the most dominant group member (the breeder male). Individuals living in large groups were overall more resistant to instability but were seemingly slower to recover from perturbation. Members of small group were more vulnerable to instability but recovered faster. Breeder females in smaller groups also showed greater physiological preparedness for instability following social perturbations. In sum, we recover both behavioral and physiological evidence that living in larger groups helps to dampen the impacts of social instability in this system.\n\nSO_SCPLOWUMMARYC_SCPLOW SO_SCPLOWTATEMENTC_SCPLOWSocial stability is vital for group productivity and long-term persistence. Here, both behavioral and physiological evidence conveys that larger groups are less susceptible to social disturbance.

animal behavior and cognition↗

Orb-weaving spiders show a correlated syndrome of morphology and web structure in the wild

Extended phenotypes are traits that exist outside the physical body of the organism. Despite their potential role in the lives of both the organisms that express them and other organisms that can be influenced by extended phenotypes, the consistency and covariance with morphological and behaviour traits of extended phenotypes is rarely evaluated, especially in wild organisms. We repeatedly measured an extended phenotype that directly influences an organisms prey acquisition, the web structure, of wild orb-weaving spiders (Micrathena vigorsii), which re-build their webs each day. We related web structure traits to behavioural traits and body size (length). Both web diameter and web density were repeatably different among individuals, while reaction to a predation threat was slightly so, but response to a prey stimulus and web symmetry were not. There was a syndrome between morphology and web structure traits, where larger spiders spun webs that were wider, had webs with increased thread spacing, and the spider tended to react more slowly to a predation threat. When a spider built a relatively larger web it was also relatively a less dense and less symmetrical web. The repeatability of web construction and relationship with spider body size we found may be common features of intra-population variation in web structure in spiders. Individual variation along the morphology and web structure syndrome could represent variation in individual foraging strategies, or age-based correlated changes. By estimating the consistency and covariances of extended phenotypes we can begin to evaluate what maintains their variation and how they might evolve.

animal behavior and cognition↗

Collective behaviour is not robust to disturbance, yet parent and offspring colonies resemble each other in social spiders

Groups of animals possess phenotypes such as collective behaviour, which may determine the fitness of group members. However, the stability and robustness to perturbations of collective phenotypes in natural conditions is not established. Furthermore, whether group phenotypes are transmitted from parent to offspring groups is required for understanding how selection on group phenotypes contributes to evolution, but parent-offspring resemblance at the group level is rarely estimated. We evaluated robustness to perturbation and parent-offspring resemblance of collective foraging aggressiveness in colonies of the social spider Anelosimus eximius. Among-colony differences in foraging aggressiveness were consistent over time but changed if the colony was perturbed through the removal of individuals, or via their removal and subsequent return. Offspring and parent colony behaviour were correlated, but only once the offspring colony had settled after being translocated. The parent-offspring resemblance was not driven by a shared elevation but could be due to other environmental factors. Laboratory collective behaviour was not correlated with behaviour in the field. Colony aggression seems sensitive to initial conditions and easily perturbed between behavioural states. Despite this sensitivity, offspring colonies have collective behaviour that resembles that of their parent colony, provided they are given enough time to settle into the environment.

evolutionary biology↗

Multilevel selection in groups of groups

Natural selection occurs at many levels. We evaluated selection acting on collectives at a level of multilevel selection analysis not yet quantified: within and between clusters of groups. We did so by monitoring the performance of natural colonies of social spiders with contrasting foraging aggressiveness in clusters of various sizes. Within-clusters, growth rates were suppressed when colonies were surrounded by more rival groups, conveying that competition is greater. When colonies were surrounded by few rivals, the more aggressive colonies in a cluster were more successful. In contrast, relatively non-aggressive colonies performed better when surrounded by many rivals. Patterns of selection between-clusters depended on the performance metric considered, but cluster-wide aggressiveness was always favored in small clusters. Together, selection both within-and between natural clusters of colonies was detectable, but highly contingent on the number of competing colonies.

evolutionary biology↗

Population differences in aggression are shaped by cyclone-induced selection

Surprisingly little is known about the evolutionary impacts of rare but extreme black swan events, like tropical cyclones. By intercepting three cyclones in fall 2018, we evaluated cyclone-induced selection on collective behavior in a group-living spider. We further examined whether historic frequencies of cyclone landfalls are correlated with geographic variation in group behavior. Cyclones consistently selected for more aggressive spider societies. Furthermore, sites where cyclones have historically been more common also harbor more aggressive groups. Thus, two corroborative lines of evidence convey that that cyclone-induced selection can drive the evolution of colony behavior, and suggest that extreme black swan events can shape within-species diversity and local adaptation.\n\nOne Sentence SummaryTropical cyclones drive the evolution of more aggressive spider societies.

ecology↗