Thomas M. Houslay

Avoiding the misuse of BLUP in behavioural ecology

Lay Summary Research of causes and consequences of animal personality promises exciting insights, yet widely used tests can lead to spurious results: when predictions of individual-level random effects are used in secondary analyses, their error is not carried forward, leading to increased likelihood of ‘false positive’ errors. We demonstrate how alternative approaches enable behavioural ecologists to test hypotheses about the causes and consequences of individual behavioural variation while accounting for the uncertainty inherent in the random effects.

Cooperative interactions within the family enhance the capacity for evolutionary change in body size

Classical models of evolution seldom predict the rate at which populations evolve in the wild. One explanation is that the social environment affects how traits change in response to natural selection. Here, we determine how social interactions between parents and offspring, and among larvae, influence the response to experimental selection on adult size. Our experiments focus on burying beetles (Nicrophorus vespilloides), whose larvae develop within a carrion nest. Some broods exclusively self-feed on the carrion while others are also fed by their parents. We found populations responded to selection for larger adults but only when parents cared for their offspring. We also found populations responded to selection for smaller adults too, but only by removing parents and causing larval interactions to exert more influence on eventual adult size. Comparative analyses revealed a similar pattern: evolutionary increases in species size within the genus Nicrophorus are associated with the obligate provision of care. Synthesising our results with previous studies, we suggest that cooperative social environments enhance the response to selection whereas excessive conflict can prevent further directional selection.

Sex differences in the effects of juvenile and adult diet on age-dependent reproductive effort

Sexual selection should cause sex differences in patterns of resource allocation. When current and future reproductive effort trade off, variation in resource acquisition might further cause sex differences in age‐dependent investment, or in sensitivity to changes in resource availability over time. However, the nature and prevalence of sex differences in age‐dependent investment remain unclear. We manipulated resource acquisition at juvenile and adult stages in decorated crickets, Gryllodes sigillatus, and assessed effects on sex‐specific allocation to age‐dependent reproductive effort (calling in males, fecundity in females) and longevity. We predicted that the resource and time demands of egg production would result in relatively consistent female strategies across treatments, whereas male investment should depend sharply on diet. Contrary to expectations, female age‐dependent reproductive effort diverged substantially across treatments, with resource‐limited females showing much lower and later investment in reproduction; the highest fecundity was associated with intermediate lifespans. In contrast, long‐lived males always signalled more than short‐lived males, and male age‐dependent reproductive effort did not depend on diet. We found consistently positive covariance between male reproductive effort and lifespan, whereas diet altered this covariance in females, revealing sex differences in the benefits of allocation to longevity. Our results support sex‐specific selection on allocation patterns, but also suggest a simpler alternative: males may use social feedback to make allocation decisions and preferentially store resources as energetic reserves in its absence. Increased calling effort with age therefore could be caused by gradual resource accumulation, heightened mortality risk over time, and a lack of feedback from available mates.

High-content analysis to leverage a robust phenotypic profiling approach to vascular modulation.

Phenotypic screening seeks to identify substances that modulate phenotypes in a desired manner with the aim of progressing first-in-class agents. Successful campaigns require physiological relevance, robust screening, and an ability to deconvolute perturbed pathways. High-content analysis (HCA) is increasingly used in cell biology and offers one approach to prosecution of phenotypic screens, but challenges exist in exploitation where data generated are high volume and complex. We combine development of an organotypic model with novel HCA tools to map phenotypic responses to pharmacological perturbations. We describe implementation for angiogenesis, a process that has long been a focus for therapeutic intervention but has lacked robust models that recapitulate more completely mechanisms involved. The study used human primary endothelial cells in co-culture with stromal fibroblasts to model multiple aspects of angiogenic signaling: cell interactions, proliferation, migration, and differentiation. Multiple quantitative descriptors were derived from automated microscopy using custom-designed algorithms. Data were extracted using a bespoke informatics platform that integrates processing, statistics, and feature display into a streamlined workflow for building and interrogating fingerprints. Ninety compounds were characterized, defining mode of action by phenotype. Our approach for assessing phenotypic outcomes in complex assay models is robust and capable of supporting a range of phenotypic screens at scale.

Vertically transmitted rhabdoviruses are found across three insect families and have dynamic interactions with their hosts

A small number of free-living viruses have been found to be obligately vertically transmitted, but it remains uncertain how widespread vertically transmitted viruses are and how quickly they can spread through host populations. Recent metagenomic studies have found several insects to be infected with sigma viruses (Rhabdoviridae). Here, we report that sigma viruses that infect Mediterranean fruit flies (Ceratitis capitata), Drosophila immigrans, and speckled wood butterflies (Pararge aegeria) are all vertically transmitted. We find patterns of vertical transmission that are consistent with those seen in Drosophila sigma viruses, with high rates of maternal transmission, and lower rates of paternal transmission. This mode of transmission allows them to spread rapidly in populations, and using viral sequence data we found the viruses in D. immigrans and C. capitata had both recently swept through host populations. The viruses were common in nature, with mean prevalences of 12% in C. capitata, 38% in D. immigrans and 74% in P. aegeria. We conclude that vertically transmitted rhabdoviruses may be widespread in a broad range of insect taxa, and that these viruses can have dynamic interactions with their hosts.

Testing the stability of behavioural coping style across stress contexts in the Trinidadian guppy

Abstract Within populations, individuals can vary in stress response, a multivariate phenomenon comprising neuroendocrine, physiological and behavioural traits. Verbal models of individual stress “coping style” have proposed that the behavioural component of this variation can be described as a single axis, with each individuals coping style being consistent across time and stress contexts. Focusing on this behavioural component of stress response and combining repeated measures of multiple traits with a novel multivariate modelling framework, we test for the existence of coping style variation and assess its stability across contexts in the Trinidadian guppy (Poecilia reticulata). Specifically, we test the following hypotheses: (1) there exists repeatable among‐individual behavioural (co)variation (“personality”) within a mild stress context consistent with a risk‐averse–risk‐prone continuum of behavioural coping style, (2) there is population‐level plasticity in behaviour as a function of stressor severity, (3) there is among‐individual variation in plasticity (i.e. IxE), and (4) the presence of IxE reduces cross‐context stability of behavioural coping style. We found significant repeatable among‐individual behavioural (co)variation in the mild stress context (open field trial), represented as an I matrix. However, I was not readily described by a simple risk‐averse–risk‐prone continuum as posited by the original coping style model. We also found strong evidence for population‐level changes in mean behaviour with increasing stressor severity (simulated avian and piscine predation risks). Single‐trait analyses did show the presence of individual‐by‐environment interactions (IxE), as among‐individual cross‐context correlations were significantly less than +1. However, multitrait analysis revealed the consequences of this plasticity variation were minimal. Specifically, we found little evidence for changes in the structure of I between mild and moderate stress contexts overall, and only minor changes between the two moderate contexts (avian vs. piscine predator). We show that a multivariate approach to assessing changes in among‐individual (co)variance across contexts can prevent the over‐interpretation of statistically significant, but small, individual‐by‐environment effects. While behavioural flexibility enables populations (and individuals) to respond rapidly to changes in the environment, multivariate personality structure can be conserved strongly across such contexts. A plain language summary is available for this article.

Mating opportunities and energetic constraints drive variation in age‐dependent sexual signalling

Summary When males repeatedly produce energetically expensive sexual signals, trade-offs between current and future investment can cause plasticity in age-dependent signalling. Such variation is often interpreted as alternate adaptive strategies: live fast and die young vs. slow and steady. An alternative (yet rarely tested) explanation is that condition-dependent constraints on allocation cause variation in signalling with age (‘late bloomers’ do not have early investment options). Testing this hypothesis is challenging because resource acquisition and allocation are difficult to measure, and energetic reserves both affect and are affected by reproductive effort. We simultaneously manipulated acquisition (through dietary nutrition) and access to potential mates (as a proxy for manipulating sexual trait allocation) in male decorated crickets (Gryllodes sigillatus), while measuring age- and signalling effort-mediated changes in energy storage components. Increased diet quality caused increased signalling effort and energy storage, while access to females increased both the likelihood of and time spent signalling. Males with lower resource budgets signalled less, but still suffered energetic storage loss and viability costs. Our results suggest that energetic constraints, rather than strategic resource accumulation, reduced signalling levels in males with lower resource acquisition ability. Our findings imply a non-adaptive explanation for age-dependent variation in sexual signalling, and an important role for energetic constraints in maintaining the honesty of costly behavioural displays. This article is protected by copyright. All rights reserved.

Host shifts result in parallel genetic changes when viruses evolve in closely related species

Host shifts, where a pathogen invades and establishes in a new host species, are a major source of emerging infectious diseases. They frequently occur between related host species and often rely on the pathogen evolving adaptations that increase their fitness in the novel host species. To investigate genetic changes in novel hosts, we experimentally evolved replicate lineages of an RNA virus (Drosophila C Virus) in 19 different species of Drosophilidae and deep sequenced the viral genomes. We found a strong pattern of parallel evolution, where viral lineages from the same host were genetically more similar to each other than to lineages from other host species. When we compared viruses that had evolved in different host species, we found that parallel genetic changes were more likely to occur if the two host species were closely related. This suggests that when a virus adapts to one host it might also become better adapted to closely related host species. This may explain in part why host shifts tend to occur between related species, and may mean that when a new pathogen appears in a given species, closely related species may become vulnerable to the new disease.

Evolutionary genetics of personality in the Trinidadian guppy II: sexual dimorphism and genotype-by-sex interactions

Sexual dimorphism in behaviour and personality has been identified in a number of species, but few studies have assessed the extent of shared genetic architecture across the sexes. Under sexually antagonistic selection, mechanisms are expected to evolve that reduce evolutionary conflict, resulting in genotype-by-sex (GxS) interactions. Here we assess the extent of sexual dimorphism in four risk-taking behaviour traits in the Trinidadian guppy, Poecilia reticulata, and apply a multivariate approach to test for GxS interactions. We also quantify the among-individual and genetic covariances between personality and size and growth, which are known a priori to differ between the sexes. We found significant sexual dimorphism in three of the four behaviours, although rmf between sex-specific homologous traits was significantly <+1 for only one behaviour. Using multivariate models, we then estimated sex-specific genetic (co)variance matrices (Gm and Gf) and tested for asymmetry of the cross-trait cross-sex genetic covariance structure (submatrix B). While Gm and Gf were not significantly different from each other overall, their respective leading eigenvectors were poorly aligned. Statistical support for asymmetry in B was found, but limited to a single trait pair for which the cross-sex covariances differed (i.e., COVA(m,f) ≠ COVA(f,m)). Thus, while single- and multi-trait perspectives evidence some GxS, the overall picture is one of similarity between the sexes in their genetic (co)variance structures. Our results suggest behavioural traits related to risk-taking may lack the sex-specific genetic architecture for further dimorphism to evolve under what is hypothesised to be antagonistic selection.

Habituation and individual variation in the endocrine stress response in the Trinidadian guppy (Poecilia reticulata) (dataset)

Highlights • Trinidadian guppies habituate quickly to repeated stress exposure.• There are strong sex differences in average cortisol release rate.• Individuals consistently differ in their average cortisol release rate.• Limited evidence for individual variation in habituation rate.