Proceedings of the Royal Society B: Biological Sciences

AbstractIridescent colours are colours that change depending on the angle of illumination or observation. They are produced when light is reflected by multilayer structures or diffracted by gratings. While this phenomenon is well understood for simple optical systems, it remains unclear how complex biological structures interact with light to produce iridescence. There are very few comparative studies at interspecific level (often focusing on a single colour patch for each species), resulting in an underestimation of structure diversity. Using an interdisciplinary approach combining physics and biology, we here quantify the colour and structure of 36 hummingbirds species evenly distributed across the phylogeny. We explore at least 2 patches per species, which are assumed to be under different selective regimes. For each patch, we measure structural features (number of layers, layer width, irregularity, spacing, etc.) of the feathers at different scales using both optical and electronic microscopy and we measure colour using a novel approach we developed to encompass the full complexity of iridescence, including its angular dependency. We discover an unsuspected diversity of structures producing iridescence in hummingbirds. We also study the effect of several structural features on the colour of the resulting signal, using both an empirical and modelling approach. Our findings demonstrate the need to take into account multiple patches per species and suggest possible evolutionary pressures causing the evolutionary transitions from one melanosome type to another.

The spectrum of light that an animal sees - from ultraviolet to far red light - is governed by the number and wavelength sensitivity of a family of retinal proteins called opsins. It has been hypothesized that the spectrum of light available in an environment influences the range of colors that a species has evolved to see. However, invertebrates and vertebrates use phylogenetically distinct opsins in their retinae, and it remains unclear whether these distinct opsins influence what animals see, or how they adapt to their light environments. Systematically utilizing published visual sensitivity data from across animal phyla, we found that terrestrial animals are more sensitive to shorter and longer wavelengths of light than aquatic animals, and that invertebrates are more sensitive to shorter wavelengths of light than vertebrates. Controlling for phylogeny removes the effects of habitat and lineage on visual sensitivity. Closed and open habitat terrestrial species have similar spectral sensitivities when comparing across the Metazoa, and deep water animals are more sensitive to shorter wavelengths of light than shallow water animals. Our results suggest that animals do adapt to their light environment, however the invertebrate-vertebrate evolutionary divergence has limited the degree to which animals can perform visual tuning.

Damselfishes (Pomacentridae) display remarkable diversity in colouration and body form, yet the processes shaping this phenotypic variation remain poorly resolved. Our study aimed to characterise the evolution of these traits, evaluate their associations with ecological factors, and identify convergent patterns linked to ecological specialisation. Using image-based quantification of colour patterns, geometric morphometrics, and phylogenetic comparative methods across 343 species, we show that pomacentrid phenotypes are organised around a small number of dominant axes describing brightness, hue, contrast, body elongation, and cranial morphology. Both colour and morphology exhibit early bursts of evolutionary disparity, followed by recurrent lineage-specific radiations and widespread convergence toward similar adaptive optima across the phylogeny. Dietary ecotypes emerged as the strongest predictor of morphological diversification, whereas symbiotic and social regimes exerted the strongest effects on colour evolution. Despite these distinct ecological correlates, several colour and shape axes form partially integrated trait syndromes that evolve in concert. The pervasive convergence of colour-shape syndromes underscores deterministic components of reef-fish evolution and positions Pomacentridae as a model for understanding integrated phenotypic evolution.

Life-history traits jointly determine survival, growth, and reproduction, yet their evolutionary interdependence remains poorly understood. Most comparative studies focus on pairwise trade-offs or composite axes, overlooking the complexity of multivariate coevolution. Here, we integrate phylogenetic path analysis and multivariate Ornstein-Uhlenbeck models to investigate the coevolution of five key life-history traits across amniotes. We show that life-history evolution proceeds through modular coevolutionary pathways with distinct tempos among traits and taxa. Despite loading similarly on the fast-slow axis of mammals and birds, clutch size and clutch frequency evolve independently at both instantaneous and long-term timescales, with clutch frequency adapting rapidly, whereas clutch size evolves slowly over macroevolutionary time. Lifespan, development time, and offspring size exhibit positive coevolution at instantaneous scales across clades, but follow distinct adaptive modes with varying directions over longer timescales. These patterns become evident only through the integrated multivariate comparative approaches.

One of the most enduring mysteries in biology concerns the evolution of complex adaptations made up of interacting component traits. When these component traits lack an obvious adaptive function in isolation from one another, their origin requires either non-adaptive, intermediate evolutionary steps or their simultaneous, synergistic evolution. We tested these alternatives using the powerful but accessible example of leaf masquerade in katydids, where in some species, highly modified wings strikingly mimic vegetation to avoid predator recognition. Combining a field predation experiment with a phylogenetic comparative analysis of wing morphology in 51 Neotropical katydid species, we show that colour and shape synergistically interact to enhance survival in the wild, and modifications in both traits evolved concurrently during diversification of this clade. Our findings identify the functionality of masquerade camouflage in the wild and highlight how synergy between individual traits fosters evolution of extraordinarily specialised adaptations.

Clownfishes (Amphiprioninae) are a fascinating example of marine radiation. From a central Pacific ancestor, they quickly colonized the coral reefs of the Indo-Pacific and diversified independently on each side of the Indo-Australian Archipelago. Their association with venomous sea anemones is often thought to be the key innovation that enabled the clownfish radiation. However, this intuition has little empirical or theoretical support given our current knowledge of the clade. To date, no ecological variable has been identified that can explain clownfish niche partitioning, phenotypic evolution, species co-occurrence, and thus, the adaptive radiation of the group. Our synthetic work solves this long-standing mystery by testing the influence of sea anemone host use on phenotypic divergence. We provide the first major revision to the known clownfish-sea anemone host associations in over 30 years, accounting for host associations in a biologically relevant way. We gathered whole-genome data for all 28 clownfish species and reconstructed a fully supported species tree for the Amphiprioninae. Integrating this new data into comparative phylogenomic approaches, we demonstrate for the first time, that the host sea anemones are the drivers of convergent evolution in clownfish color pattern and morphology. During the adaptive radiation of this group, clownfishes in different regions that associate with the same hosts have evolved the same phenotypes. Comparative genomics also reveals several genes under convergent positive selection linked to host specialisation events. Our results identify the sea anemone host as the key ecological variable that disentangles the entire adaptive radiation. As one of the most recognizable animals on the planet and an emerging model organism in the biological sciences, our findings bear on the interpretation of dozens of prior studies on clownfishes and will radically reshape research agendas for these iconic organisms.

Species interactions have evolved from antagonistic to mutualistic and back several times throughout lifes history. Yet, it is unclear how changes in the type of interaction between species alter the coevolutionary dynamics of entire communities. This is a pressing matter, as transitions from mutualisms to antagonisms may be becoming more common with human-induced global change. Here, we combine network and evolutionary theory to simulate how shifts in interaction types alter the coevolution of empirical communities. We show that as mutualistic networks shift to antagonistic, selection imposed by direct partners begins to outweigh that imposed by indirect partners. This weakening of indirect effects is associated with communities losing their tight integration of traits and increasing their rate of adaptation. The above changes are more pronounced when specialist consumers are the first species to switch to antagonism. A shift in the outcome of species interactions may therefore reverberate across communities and alter the direction and speed of coevolution.

Climate change is causing extreme heating events. Simultaneously, climate change and human activities are leading to more prolonged and intense infectious disease outbreaks. The extent to which warming and infection may together impact host species persistence is, however, unclear. Using a meta-analysis of >190 effect sizes representing 101 ectothermic animal host-pathogen systems, we provide broad evidence that experimentally increased temperatures drove higher pathogen virulence, specifically pathogen-induced host mortality. Such pattern was mainly driven by excess host death caused by bacterial infections combined with warming, particularly if the pathogenic bacteria were naturally established within the host species, though novel infections without known host-pathogen evolutionary history were more lethal at lower temperatures. Importantly, larger temperature increases were associated with more host deaths hinting at the escalating threat for animal species as the world continues to warm. We found that the virulence of fungal pathogens increased only when temperatures were shifted upwards towards their thermal optimum. The magnitude of these effects was not impacted by host life-stage, immune complexity, or variable experimental protocols. Overall, our findings reveal distinct patterns of pathogen virulence change under warmer temperatures, suggesting that the impact of global warming on infectious disease outcomes would depend on pathogen traits (taxonomic kingdom, thermal tolerance) and host-pathogen evolutionary history. Author SummaryHuman-induced climate warming is one of the biggest challenges in our times. Simultaneously, climate change is associated with more intense infectious disease outbreaks, suggesting that temperature rises also influence disease dynamics. Growing numbers of studies have investigated the effect of warming on disease severity (or pathogen virulence) in different animal host-pathogen systems. However, individual studies did not always agree with each other, and how increased temperature and pathogen infection together impact animal survival remains unclear. Here, we resolved this uncertainty by conducting a meta-analysis of >190 effect sizes representing 101 animal host-pathogen systems. We provided broad evidence that, higher temperatures caused more deaths of infected animals, particularly for animals with bacterial infections under warmer conditions. We found that larger temperature rises were associated with more animal deaths, suggesting the increased threat for host species as the world continues to warm. We also found that pathogenic fungi were more sensitive to heat than bacterial pathogens, and temperature changes the virulence of fungal pathogens in relation to their thermal optimum.

Avian brood parasitism is a well-recognized model for studying coevolution. In this model, hosts adapt the ability to recognize and remove parasitic young to avoid the costs of rearing foreign offspring, while parasites counter-adapt phenotypes to evade detection. A classic example of host-parasite coevolutionary arms race is the great reed warbler and its parasite the common cuckoo (hereafter warbler and cuckoo, respectively). Recent work has found that cuckoo eggs are more likely to be accepted by warblers when those are bluer than their own eggs. Therefore, hosts would select for bluer cuckoo eggs; in turn, this provides directional selection for hosts eggs to remain bluer than cuckoo eggs. Here, we tested whether there were consistent differences in eggshell appearance between cuckoo and warbler eggs using a dataset which provides eggshell coloration of both warblers and cuckoos from the same nest. Despite being a textbook example of mimicry, we found that the cuckoos have significantly browner eggs than the warblers. These findings most likely suggest that this warbler-cuckoo system is experiencing negative frequency-dependent selection, as expected under red queen dynamics. Future research comparing warbler-cuckoo interactions over time would advance our understanding of the coevolution between avian brood parasites and their hosts.

The length of gestation in eutherian mammals, which is key to their reproductive success, is closely connected to other life history traits and with body mass and brain mass, but causal relationships between these variables are unclear. Here, we used an integrative analytical framework to evaluate the evolutionary relationships between gestation length and eight other traits on a dataset of 3,258 eutherian mammals and infer causality. We identify variation in generation length and litter size as the primary predictors of eutherian gestation length variation, whereas additional traits, such as brain mass, significantly predict gestation length only in specific mammalian orders. Using a structural equation modeling approach known as phylogenetic path analysis to infer causality, we find that gestation length variation positively influences brain mass variation and negatively influences litter size variation. Furthermore, body mass causally influences gestation length variation only in certain orders. Consistent with these causal inferences, examination of trait-trait coevolution reinforces that gestation length is strongly positively associated with brain mass, strongly negatively associated with litter size, and only moderately correlated with body mass. These findings reveal how gestation length directly and indirectly influences, and is influenced by, other key eutherian traits. Our study establishes a robust framework for identifying causal relationships within suites of correlated and co-evolving traits.

Animals respond to competition among kin for critical breeding resources in two ways: avoidance of direct fitness costs via dispersal of siblings to breed separately, and formation of kin-based societies in which subordinates offset direct fitness costs of breeding competition via altruism and increased indirect fitness. Here we provide the first evidence that kin competition can promote the evolution of societies based on non-kin cooperation. For eastern carpenter bees, nests are a critical breeding resource in perpetually short supply, leading to strong competition among females. Observations of individually marked and genotyped females demonstrate that sisters disperse from their natal nests to join social groups of nonrelatives. By forming social groups of non-kin, females increase their chances of successful reproduction, while avoiding the indirect fitness cost of competition among sisters. One Sentence SummaryWe describe the first known example of an animal society based on avoidance of kin competition rather than on promotion of kin cooperation.

Acoustic signal complexity varies widely in the animal kingdom for reasons that remain unclear. In birds, it is widely proposed that vocal complexity evolves as an honest signal of individual quality driven by sexual selection. Other hypotheses related to social interactions include competition for ecological resources (social selection) and intra-group communication in group- living animals, both of which may favour signal complexity. However, these hypotheses are rarely explored at macroevolutionary scales, particularly in the context of constraints on sound production, transmission and detection, leading to ongoing uncertainty about the evolutionary origins of complex vocal signals. Using Bayesian phylogenetic models, we test whether different forms of social communication and ecological constraints predict the temporal and spectral complexity of songs in 1,288 species of suboscine passerine birds. We found that song complexity was reduced by sexual selection, along with other limiting factors including large body size and dense vegetation. Conversely, territoriality boosted the temporal complexity of songs. These findings challenge the common assumption that sexual selection is the main driver of increased signal complexity, and instead highlight the role of social selection as a key component of multiple inter-related drivers and constraints.

Complex colour pattern traits often evolve in response to multiple selective pressures, emphasizing the need for their investigation in an integrative framework. We use museum specimens (n=718) to study the evolution of coat colouration in three palm squirrel species (Funambulus spp.) in the Indian subcontinent, with climate, vegetation, and predators as the potential selective forces. Our results indicate a strong geographical trend in coat colour distribution within and across species, with darker individuals in the southern and lighter individuals in the northern regions. We find significant darkening of coat colouration in more humid, densely vegetated regions with dark soils. Fine-scale intra-specific analyses suggest that species respond differently to multiple abiotic selective pressures. Investigation of stripe pattern elements suggests that the colour-based elements are more visible to raptors, while luminance-based elements are more visible to ferrets. We also find that squirrel species are darker in areas with denser and taller canopies, with low-contrast stripes specific to each predators vision. Overall, squirrel coat colouration evolves in response to multiple abiotic factors, including climate and habitat, and specific stripe elements provide particular visual effects on predators depending on the habitat.

The ecology of fear demonstrates how prey responses to avoid predation cause non-lethal effects at all ecological scales. Parasites also elicit defensive responses in hosts with associated non-lethal effects, which raises the longstanding, yet unresolved question of how non-lethal effects of parasites compare with those of predators. We developed a framework for systematically answering this question for all types of predator and parasite systems. Our framework predicts that trait responses and their non-lethal effects should be strongest from predators and parasites that do not kill individuals to feed on them, but which nevertheless damage fitness. Analysing trait response data on amphibians, which have been well-studied for this area of research, showed that individuals generally responded more directly to short-term predation risks than to parasitism. Apart from studies using amphibians, there have been few direct comparisons of responses to predation and parasitism, and none have incorporated responses to micropredators, parasitoids, or parasitic castrators, or examined their long-term consequences. Addressing these and other data gaps highlighted by our general framework can advance the field toward understanding how non-lethal effects shape real food webs, which contain multiple predator and parasite species.

When males compete, sexual selection favors reproductive traits that increase their mating or fertilization success (pre- and post-copulatory sexual selection). It is assumed that males face a trade-off between these two types of sexual traits because they both draw on investment from the same pool of resources. Consequently, investment into mate acquisition or ejaculation should create similar trade-offs with other key life history traits. Tests of these assumptions are exceedingly rare. Males only ejaculate after they mate, and investment into ejaculation is therefore highly correlated with mating effort. Consequently, little is known about how each component of reproductive investment affects a males future performance. Here, we ran an experiment using a novel technique to distinguish the life history costs of mating effort and ejaculation for mosquitofish (Gambusia holbrooki). We compared manipulated males (mate without ejaculation), control males (mate and ejaculate) and naive males (neither mate nor ejaculate) continuously housed with a female and two rival males. We assessed their growth, somatic maintenance, mating and fighting behavior, and sperm traits after 8 and 16 weeks. Past mating effort significantly lowered a males future mating effort and growth, but not his sperm production; while past sperm release significantly lowered a males future ejaculate quantity, but not his mating effort. These findings challenge the assumption that male reproductive investment draws from a common pool of resources such that, all else being equal, greater mating effort reduces ejaculate investment, and vice versa. Instead, we provide clear evidence that investment in traits under pre- and post-copulatory sexual selection have different trait-specific effects on subsequent male reproductive performance that occur both early and late in life.

In contrast to most butterflies harboring opaque wing colorations, some species display large transparent patches on their wings. Wing transparency, which entails a dramatic reduction of pigmentation, raises the question of potential costs for vital functions, such as thermoregulation, especially along climatic gradients. The thermal melanism hypothesis posits that darker colorations should be favored in colder environments, which enables them to absorb more radiation and maintain a body temperature compatible with activity. This prediction extends to the near infrared (NIR) range, which represents a large proportion of solar radiation. Here we assess the implications of wing transparency for light absorption and thermal properties in 42 butterfly species from the neotropical tribe Ithomiini that range the extent of transparency, from fully opaque to highly transparent, and we test whether those species conform to the prediction of the thermal melanism hypothesis. We find that transparent wings are less efficient than opaque wings to absorb light across UV, Visible and NIR wavelength ranges, and are also less efficient to collect heat. Moreover, dark coloration occupies a lower proportion of wing area as altitude increases, and ithomiine species harbor more transparency at higher altitudes, where climatic conditions are colder, going strongly against the prediction of the thermal melanism hypothesis. We discuss these surprising results in light of recent studies suggesting that factors other than adaptation to cold, such as predation pressure, physiology or behavior, may have driven the evolution of wing patterns in Ithomiini. Significance StatementThe thermal melanism hypothesis predicts that organisms should be darker and absorb solar radiation more efficiently in colder environments. The Neotropical butterflies Ithomiini are unusual in that many species harbor large transparent patches on their wings, raising questions related to their efficacy of solar radiation absorption and heating capacities. We investigate optical and thermal properties of several ithomiine species along a climatic gradient. We find that transparent wings are less efficient at absorbing radiation and collecting heat. Unexpectedly, the proportion of transparent species increases with altitude, challenging the thermal melanism hypothesis and suggesting that factors other than adaptation to cold, such as predation pressure, may have driven the evolution of wing patterns in Ithomiini.

The evolutionary mechanisms of cooperation are well-studied, yet what motivates individuals to cooperate remains unclear. Although conventionally associated with enhanced social tolerance (self-domestication hypothesis) and prosociality (cooperative-breeding hypothesis), individuals belonging to species that are neither self-domesticated nor cooperatively-breeding also cooperate. An overarching interdependency hypothesis posits that inter-individual dependencies promote cooperation, but comparative evidence is lacking. We experimentally studied cooperation, prosociality, and tolerance in six macaque species along a despotic-egalitarian gradient. Within-group cooperation was higher in despotic than egalitarian societies yet restricted to few partners. Prosociality, kinship, and tolerance positively predicted cooperation success. Agent-based models consistently showed that despotic societies have fewer but more stable social bonds and, thus, higher interdependencies than egalitarian ones. Our results suggest that interdependencies facilitate the emergence and maintenance of cooperation.

Early life environments can have long-lasting effects on adult reproductive performance, but disentangling the influence of early and adult life environments on fitness is challenging, especially for long-lived species. Using a detailed dataset spanning over two centuries, we studied how early and adult life environments impact reproductive performance in preindustrial women. We assessed the effect of environmental conditions associated with the parish of birth and the parish where the women had their offspring. We considered resource availability differences between rural, urban, northern, and southern parishes by comparing women who switched environments during their lifetime with those who did not. We found that urban-born women had an earlier age at first reproduction and lower offspring survival to adulthood than rural-born women, while South Quebec women had more offspring born than North Quebec women. Moreover, switching from urban to rural led to higher offspring survival, while the reverse had the opposite effect. In addition, moving from South to North resulted in fewer offspring born and surviving, whereas moving from North to South had the inverse effect. Finally, women who changed from rural to urban and from South to North had their first child at an older age compared to those who stayed in the same urbanity type. Our study underscores the complex and interactive effects of early and adult life environments on reproductive traits, highlighting the need to consider both when studying environmental effects on reproductive outcomes.

AbstractExplaining the evolution of sex differences in cooperation remains a major challenge. Comparative studies highlight that offspring of the more philopatric sex tend to be more cooperative within their family groups than those of the more dispersive sex but we do not understand why. The leading Philopatry hypothesis proposes that the more philopatric sex cooperates more because their higher likelihood of natal breeding increases the direct fitness benefits of natal cooperation. However, the Dispersal trade-off hypothesis proposes that the more dispersive sex cooperates less because preparations for dispersal, such as extra-territorial prospecting, trade-off against natal cooperation. Here, we test both hypotheses in cooperatively breeding white-browed sparrow weavers (Plocepasser mahali), using a novel high-resolution automated radio-tracking method. First, we show that males are the more dispersive sex (a rare reversal of the typical avian sex-difference in dispersal) and that, consistent with the predictions of both hypotheses, females contribute substantially more than males to cooperative care while within the natal group. However, the Philopatry hypothesis cannot readily explain this female-biased cooperation, as females are not more likely than males to breed within their natal group. Instead, our radio-tracking findings support the Dispersal trade-off hypothesis: males conduct pre-dispersal extra-territorial prospecting forays at higher rates than females and prospecting appears to trade-off against natal cooperation. Our findings thus highlight that the evolution of sex differences in cooperation could be widely attributable to trade-offs between cooperation and dispersal; a potentially general explanation that does not demand that cooperation yields direct fitness benefits.

The selective factors that shape phenotypic diversity in prey communities with aposematic animals are diverse and coincide with similar diversity in the strength of underlying secondary defences. However, quantitative assessments of colour pattern variation and the strength of chemical defences in assemblages of aposematic species are lacking. We quantified colour pattern diversity using Quantitative Colour Pattern Analysis (QCPA) in 13 Dorid nudibranch species (Infraorder: Doridoidei) that varied in the strength of their chemical defences. We accounted for the physiological properties of a potential predators visual system (a triggerfish, Rhinecanthus aculeatus) and modelled the appearance of nudibranchs from multiple viewing distances (2cm and 10cm). We identified distinct colour pattern properties associated with the presence and strength of chemical defences. Colour patterns were also less variable among species with chemical defences when compared to undefended species. This confirms correlations between secondary defences and diverse, bold colouration while showing that chemical defences coincide with decreased colour pattern variability among species. Our study suggests that complex spatiochromatic properties of colour patterns perceived by potential predators can be used to make inferences on the presence and strength of chemical defences.