The evolution and ecology of multiple antipredator defences.

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such "defence portfolios" that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.

Prior experience of captivity affects behavioural responses to 'novel' environments.

Information ecology theory predicts that prior experience influences current behaviour, even if the information is acquired under a different context. However, when individuals are tested to quantify personality, cognition, or stress, we usually assume that the novelty of the test is consistent among individuals. Surprisingly, this 'gambit of prior experience' has rarely been explored. Therefore, here we make use of a wild population of great tits (Parus major) to test if prior experience of handling and captivity influences common measures of exploration (open field tests in two novel contexts: room and cage arenas), social response (simulated using a mirror), and behavioural stress (breathing rate). We found that birds with prior experience of captivity (caught previously for unrelated learning and foraging experiments) were more exploratory, but this depended on age: exploration and captivity experience (in terms of both absolute binary experience and the length of time spent in captivity) were associated more strongly in young (first-winter) birds than in adults. However, there was no association of prior experience of captivity with social response and breathing rate, and nor did the measures of exploration correlate. Together our results suggest that re-testing of individuals requires careful consideration, particularly for younger birds, and previous experiences can carry over and affect behaviours differently.

A Chromosome-Level Genome Assembly of the Reed Warbler (Acrocephalus scirpaceus).

The reed warbler (Acrocephalus scirpaceus) is a long-distance migrant passerine with a wide distribution across Eurasia. This species has fascinated researchers for decades, especially its role as host of a brood parasite, and its capacity for rapid phenotypic change in the face of climate change. Currently, it is expanding its range northwards in Europe, and is altering its migratory behavior in certain areas. Thus, there is great potential to discover signs of recent evolution and its impact on the genomic composition of the reed warbler. Here, we present a high-quality reference genome for the reed warbler, based on PacBio, 10×, and Hi-C sequencing. The genome has an assembly size of 1,075,083,815 bp with a scaffold N50 of 74,438,198 bp and a contig N50 of 12,742,779 bp. BUSCO analysis using aves_odb10 as a model showed that 95.7% of BUSCO genes were complete. We found unequivocal evidence of two separate macrochromosomal fusions in the reed warbler genome, in addition to the previously identified fusion between chromosome Z and a part of chromosome 4A in the Sylvioidea superfamily. We annotated 14,645 protein-coding genes, and a BUSCO analysis of the protein sequences indicated 97.5% completeness. This reference genome will serve as an important resource, and will provide new insights into the genomic effects of evolutionary drivers such as coevolution, range expansion, and adaptations to climate change, as well as chromosomal rearrangements in birds.

Geographic mosaic of selection by avian predators on hindwing warning colour in a polymorphic aposematic moth.

Warning signals are predicted to develop signal monomorphism via positive frequency-dependent selection (+FDS) albeit many aposematic systems exhibit signal polymorphism. To understand this mismatch, we conducted a large-scale predation experiment in four countries, among which the frequencies of hindwing warning coloration of the aposematic moth, Arctia plantaginis, differ. Here we show that selection by avian predators on warning colour is predicted by local morph frequency and predator community composition. We found +FDS to be the strongest in monomorphic Scotland and lowest in polymorphic Finland, where the attack risk of moth morphs depended on the local avian community. +FDS was also found where the predator community was the least diverse (Georgia), whereas in the most diverse avian community (Estonia), hardly any models were attacked. Our results support the idea that spatial variation in predator communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection.

Diversity in warning coloration: selective paradox or the norm?

Aposematic theory has historically predicted that predators should select for warning signals to converge on a single form, as a result of frequency-dependent learning. However, widespread variation in warning signals is observed across closely related species, populations and, most problematically for evolutionary biologists, among individuals in the same population. Recent research has yielded an increased awareness of this diversity, challenging the paradigm of signal monomorphy in aposematic animals. Here we provide a comprehensive synthesis of these disparate lines of investigation, identifying within them three broad classes of explanation for variation in aposematic warning signals: genetic mechanisms, differences among predators and predator behaviour, and alternative selection pressures upon the signal. The mechanisms producing warning coloration are also important. Detailed studies of the genetic basis of warning signals in some species, most notably Heliconius butterflies, are beginning to shed light on the genetic architecture facilitating or limiting key processes such as the evolution and maintenance of polymorphisms, hybridisation, and speciation. Work on predator behaviour is changing our perception of the predator community as a single homogenous selective agent, emphasising the dynamic nature of predator-prey interactions. Predator variability in a range of factors (e.g. perceptual abilities, tolerance to chemical defences, and individual motivation), suggests that the role of predators is more complicated than previously appreciated. With complex selection regimes at work, polytypisms and polymorphisms may even occur in Müllerian mimicry systems. Meanwhile, phenotypes are often multifunctional, and thus subject to additional biotic and abiotic selection pressures. Some of these selective pressures, primarily sexual selection and thermoregulation, have received considerable attention, while others, such as disease risk and parental effects, offer promising avenues to explore. As well as reviewing the existing evidence from both empirical studies and theoretical modelling, we highlight hypotheses that could benefit from further investigation in aposematic species. Finally by collating known instances of variation in warning signals, we provide a valuable resource for understanding the taxonomic spread of diversity in aposematic signalling and with which to direct future research. A greater appreciation of the extent of variation in aposematic species, and of the selective pressures and constraints which contribute to this once-paradoxical phenomenon, yields a new perspective for the field of aposematic signalling.

The dual role of rivers in facilitating or hindering movements of the false heath fritillary butterfly.

BACKGROUND: Species movement responses to landscape structures have been studied using a variety of methods, but movement research is still in need of simple methods that help predicting and comparing movements across structurally different landscapes. We demonstrate how habitat-specific movement models can be used to disentangle causes of differentiated movement patterns in structurally different landscapes and to predict movement patterns in altered and artificial landscapes. In our case study, we studied the role of riparian landscapes to the persistence of the endangered false heath fritillary butterfly (Melitaea diamina) in its newly discovered coastal distribution region in Finland. We compared the movement parameters of the riparian population to two reference populations by using capture-recapture data and habitat-specific diffusion modelling, and analysed the role of the river and riverbank buffer zones in facilitating or hindering false heath fritillary movement with movement simulations. RESULTS: The riparian population of the false heath fritillary did not show major differences to reference populations in terms of movement parameters within breeding habitat, high-quality matrix and low-quality matrix. However, movement simulations showed that the habitat-specific movement parameters estimated for the false heath fritillary can lead into markedly different movement patterns in structurally different landscapes. An artificial riparian landscape mimicking those of the coastal distribution resulted into more directional, longitudinal movements both parallel and perpendicular to the river than a more mosaic-like landscape, but the existence of the river in the landscape reduced movements across the river. CONCLUSIONS: Our study demonstrates how habitat-specific movement models enable comparisons of movement patterns across structurally different real, altered and artificial landscapes. As such, they can be used to compare movement parameters across populations, to study the effects of management interventions to endangered species and to identify areas that have high sensitivity to individual movement. In our case study, the river is shown to perform a dual role for the movements of the riparian false heath fritillary population. Whereas the river acts as a moderate movement barrier for the false heath fritillary, the longitudinal configuration of riverbank habitats provides a means especially for the male false heath fritillaries to move across the landscape.