Biological Reviews

Social factors have been argued to be the main selection pressure for the evolution of large brains and complex behavior on the basis of data from mammals and birds. Coleoid cephalopods (octopuses, squid, and cuttlefish) have large brains, complex nervous systems and show signs of intelligent behavior comparable to that of primates, cetaceans, and birds. However, many cephalopods live largely solitary, semelparous, short lives, and many are cannibalistic, leaving little to no opportunity for parental care, complex group dynamics, or social learning. This suggests that the large brains found in cephalopods are not the result of social selection pressures. Here, motivated by the predictions of the "Asocial Brain Hypothesis", a yet untested regime of the Cultural Brain Hypothesis formal model, we compare the relationships between brain size and social, ecological, and other factors in cephalopods. Consistent with the prediction that ecological factors should be the primary selection pressure with larger brains in more calorie-rich complex ecologies, we find that shallower and benthic (seafloor) habitats--arguably more complex environments than open-ocean (pelagic) habitats--are associated with larger brain sizes, and that measures of sociality are not. Our findings from these highly divergent evolutionary lineages, which diverged from vertebrates over 500 million years ago are not causal, but are consistent with the "Asocial Brain Hypothesis" mechanistic model that describes how ecological selection pressures can also produce large, complex brains.

Animals communicate acoustically to report location and identity to conspecifics. More complex patterning of calls can also function as displays to potential mates and as territorial advertisement. Music and song are terms often reserved only for humans and birds, but elements of both forms of acoustic display are also found in non-human primates. While theories on proximate functions abound, ultimate drivers of specific call structures are less well understood. We hypothesized that spatio-temporal precision in landing during perilous arboreal locomotion favored the evolution of musical calling in early primates--vastly preceding the origin of more music-like behavior in hominoids and subsequent emergence of music in later hominids. We test this locomotion-based hypothesis on the origins of proto-musicality using spectrographic depictions of vocal repertoires of modern day primates and corresponding estimates of locomotor activity. Phylogenetically controlled regression analysis of 54 primate species reveals that arboreal locomotion and monogamy are robust influences on complex calling patterns while controlling for other socioecological variables. Given that these findings rest primarily upon a handful of deep branching points in the primate tree, we conclude that this coevolution likely occurred very slowly, occupying on the order of tens of millions of years. LicenseAttribution-NoDerivatives 4.0 International (CC BY-ND 4.0)

Vocal production learning (VPL), the capacity to imitate sounds, is a crucial, but not exclusive component of human language. VPL is rare in animals but common in birds, where it evolved independently in songbirds, hummingbirds, and parrots. Parrots (Psittaciformes) learn new vocalizations throughout their lives and exhibit astonishing vocal flexibility and imitation capacity. They can copy allospecific sounds, e.g., human words and learn their associated meanings. Parrots, therefore, present an intriguing model to shed light on how VPL evolved and how it may relate to other language-relevant traits. How widely VPL is distributed across Psittaciformes and to what extent (qualitative) species differences exist, remains unknown. Here, we provide the first comprehensive overview of the phylogenetic distribution of (allospecific) VPL in this clade by conducting surveys of publicly available video footage. Out of the 398 currently recognized extant species, we found videos for 163, of which 136 showed evidence of VPL. Phylogenetic analyses suggest secondary losses and reacquisitions of VPL covarying with socioecological parameters (gregariousness), life-history (longevity), and morphological (body size) traits. This study provides the first insights into interspecific variation in vocal learning across all parrot species and reveals potential socio-ecological drivers of its evolution. SignificanceLittle is known about the selective forces that favor the evolution of vocal production learning (VPL), a rare trait in animals and a prerequisite for the evolution of human language. We provide the first insights into interspecific variation in VPL in the evolutionary history of parrots and uncover candidate evolutionary drivers. The current data suggest that the evolution of VPL within parrots has been highly dynamic, with multiple secondary losses and reacquisitions. Our model showed that VPL most likely was the ancestral state. Sociality, longevity and body size explain variation in VPL together with a highly uncertain effect of brain size. The findings may motivate comparative work in other taxa and contribute to research into the evolutionary origins of human language.

The Cooperative Eye Hypothesis (CEH) and the Gaze-Signalling Hypothesis (GSH) propose that the human eye--distinguished by pronounced scleral exposure and a uniformly white sclera-- evolved as a unique trait among primates to enhance eye-gaze visibility and facilitate cooperative communication. A recent review by Perea-Garcia and colleagues (2025) questioned four central premises of these hypotheses: (1) that human eye morphology is unique among primates, (2) that it is expressed consistently across individuals and populations, (3) that it improves gaze-following, and (4) that it is linked to the evolution of social cognition. Here, we revisit each claim through reevaluation of evidence and reanalysis of published data. First, we show that although some primates exhibit scleral depigmentation, humans uniquely combine this with high scleral exposure, resulting in markedly greater gaze visibility. Second, despite variation in scleral brightness, cross-species comparisons of sclera-iris-skin contrast confirm that human eyes remain distinct from those of other closely related apes. Third, experimental studies demonstrate that the white sclera confers a clear communicative advantage under ecologically relevant conditions, and that only humans consistently exploit these cues. Finally, developmental, cross-cultural, and neurocognitive evidence indicates that humans possess dedicated perceptual mechanisms for eye-gaze, consistent with its evolutionary embedding in social cognition. We conclude that while claims of human uniqueness should be moderated, the CEH and GSH remain the most plausible explanations for the evolution of human eye morphology. We also highlight key directions for future behavioral, anatomical, and genetic research.

There may be fitness tradeoffs between wound healing, immune responses, and cancer development due to shared pathways, limited resources and conflicting selective pressures. The immune system is important in both response to injury and carcinogenesis. We initially investigated correlations between cancer prevalence and immune cells, controlling for known associations with body mass and lifespan. We analyzed data from 216 mammalian species from at least 20 individuals per species. Body mass correlated positively with segmented neutrophil-to-lymphocyte ratios and negatively with lymphocyte concentrations. However, only platelet concentration correlated (negatively) with cancer prevalence (P-value = 0.006). To further understand this association, we investigated whether a fitness tradeoff could exist between preventing death from cancer versus injury. We discovered a negative correlation between cancer and trauma mortalities (P-value [≤] 0.0006), even when we accounted for the fact that different causes of death must sum to 100%. Platelet size and trophic level negatively correlated with trauma mortality, but not when controlling for cancer mortality (P-value = 0.06). If trauma mortality is an indirect measure of wound healing, this suggests a fitness tradeoff may exist between cancer suppression and wound healing across mammals, mediated in part through platelet size and trophic level.

It is widely assumed that the first placental mammals were solitary. This assumption has been used as the default in previous comparative studies, but has never been tested independently. Here, we compiled a comprehensive database by reviewing over 14,000 primary peer-reviewed publications on the social organization of the 5,386 extant placental mammal species. We found empirical data for 738 species across 1,478 populations: 354 populations were primarily solitary, 241 populations pair-living and 878 populations group-living. Notably, 383 species (52%) and 580 populations (39%) exhibited intra-specific variation in social organization. Using a Bayesian phylogenetic framework that incorporates intra-specific variation, we show that the ancestral placental mammal - living approximately 160 to 100 million years ago - was not exclusively solitary, but likely displayed intraspecific variation. Pair-living was predicted to account for approximately 26% of ancestral social organisation. Our analysis found that ecology and life history of extant solitary and pair-living mammals was very similar and different from those of group-living mammals. Our results revise prevailing theories of mammalian social evolution, revealing that pair-living emerged early, shifting the focus of mammalian social evolution from the origins of pair-living to the origins of group-living.

Billions of animals across many taxa are extensively farmed, with critical impacts on animal welfare. Societal efforts to reduce animal suffering lack rigorous and systematic approaches that facilitate maximising welfare improvements, such as informed funding allocation decisions. We present a multi-measure, cross-taxa framework for modelling differences in pain, suffering, and related cognition to assess whether certain animals have larger welfare ranges (how well or badly animals can fare). Measures include behavioural flexibility, cognitive sophistication, and general learning. We evaluated 90 empirically detectable proxies for cognition and welfare range (henceforth proxies) in pigs, chickens, carp, salmon, octopus, shrimp, crabs, crayfish, bees, and silkworms. We grouped a subset of proxies into: A) 10 ideal proxies and B) 10 less ideal proxies but with sufficient data for interspecies comparisons. We graded the strength of evidence per proxy across taxa, and constructed a cognition and welfare range profile, with overall judgement scores (ranging from likely no/low confidence to yes/very high confidence). We discuss the implications of comparisons and highlight key avenues for future research. This work is timely, given recent indications of significant political will towards reducing animal suffering, such as the inclusion of cephalopods and decapods in the Animal Welfare (Sentience) Bill following a UK government-commissioned research review. Given the novelty and robustness of our review, we believe it sets a new standard for investigating interspecies comparisons of cognition and welfare ranges and helps inform future research. This should help streamline funding allocations and improve the welfare of millions of farmed animals. Graphical/ Visual Abstract and Caption O_FIG_DISPLAY_L [Figure 1] M_FIG_DISPLAY Cognition and welfare in farmed animals - from pigs to silkworms (Free stock images: http://www.pixabay.com) C_FIG_DISPLAY

Highly pathogenic avian influenza (HPAI) has become a critical threat to wildlife, shifting from a seasonal epizootic to a persistent, year-round panzootic with global consequences. Here, we summarize the origin, evolutionary mechanisms, and expanding host range of the current H5N1 virus (clade 2.3.4.4b) and assess its impact on wildlife. Over the past five years, HPAI has caused the deaths of millions of wild birds, causing dramatic population declines in several seabird species. However, comprehensive quantitative mortality data remain scarce, as existing records are often anecdotal, focus on localized mass die-offs, and thus represent only a fraction of the true magnitude of mortality. This gap in data limits the ability to predict outbreak dynamics and mitigate long-term consequences. Using the Northwestern European Sandwich Tern (Thalasseus sandvicensis) population as a case study, we demonstrate the value of integrating mortality data with ecological, serological and genetic data before, during and after an outbreak. This approach uncovered age-specific vulnerability, selective mortality, and population immunological responses. In addition, insights gained with respect to the role of breeding density, carcass removal, and host adaptation in modulating outbreak dynamics are likely to be generalizable across seabird species. The absence of a centralized and standardized wildlife mortality monitoring framework, on the other hand, remains a major barrier to effective outbreak forecasting and conservation planning. We argue that integrating field-based mortality data, population monitoring, serological assays, and genetic analyses within a One Health framework is essential to enable early detection, targeted mitigation, and robust evaluation of outbreak impacts. Without a proactive and data-driven approach to conservation, HPAI will continue to threaten global wildlife populations, with cascading ecological, economic and public health consequences.

A critical review of alternative grazing strategies and their impact on soil organic carbon (SOC) found most studies (n = 47) failed minimum quality criteria. Ten rigorous studies showed no significant SOC change, yet thirteen less robust studies suggested SOC increases. This divergence highlights that low-quality evidence is prevalent, underscoring a critical need for stronger evidence before asserting climate change mitigation benefits from alternative grazing practices.

Colonization of a novel habitat is often followed by radiation in the wake of ecological opportunity. Alternatively, some habitats should be inherently more constraining than others if the challenges of that environment have few evolutionary solutions. We examined the push-and-pull of these factors on evolution following habitat transitions, using anglerfishes (Lophiiformes) as a model. Deep-sea fishes are notoriously difficult to study, and poor sampling has limited progress thus far. Here we present a new phylogeny of anglerfishes with unprecedented taxonomic sampling (1,092 loci and 40% of species), combined with three-dimensional phenotypic data from museum specimens obtained with micro-CT scanning. We use these datasets to examine the tempo and mode of phenotypic and lineage diversification using phylogenetic comparative methods, comparing lineages in shallow and deep benthic versus bathypelagic habitats. Our results show that anglerfishes represent a surprising case where the bathypelagic lineage has greater taxonomic and phenotypic diversity than coastal benthic relatives. This defies expectations based on ecological principles since the bathypelagic zone is the most homogeneous habitat on Earth. Deep-sea anglerfishes experienced rapid lineage diversification concomitant with colonization of the bathypelagic zone from a continental slope ancestor. They display the highest body, skull and jaw shape disparity across lophiiforms. In contrast, reef-associated taxa show strong constraints on shape and low evolutionary rates, contradicting patterns suggested by other shallow marine fishes. We found that Lophiiformes as a whole evolved under an early burst model with subclades occupying distinct body shapes. We further discuss to what extent the bathypelagic clade is a secondary adaptive radiation, or if its diversity can be explained by non-adaptive processes.

Biodiversity dynamics following encounters between long-isolated faunas provide natural experiments to examine how diversity dependence and ecological interactions shape diversification patterns at macroevolutionary time scales. The Cenozoic arrival of African and North American mammals in South America likely had transformative effects on one of the worlds most unique and previously isolated continental faunas. However, the extent and persistence of these effects remain debated. Here, we assess the impact of immigrant mammal groups on native South American mammal diversity by combining an extensive fossil dataset (6,214 occurrences; 1,739 species) with deep learning methods and time-series analyses to model dynamics of mammalian biodiversity throughout the Cenozoic. The arrival of African and North American lineages increased the continents overall species richness but also contributed to a decline in native diversity. Additionally, our models suggest that the negative effect of immigrant lineages on native diversity was strongest immediately after their arrival and initial diversification, but this effect lessened over time. Overall, these findings support a scenario where immigration simultaneously enriched South American faunas and triggered a time-decaying replacement of native lineages, reshaping continental biodiversity.

Reproductive seasonality offsets the energetic costs of reproduction by synchronizing births with peak resources and is traditionally expected to increase with latitude and environmental seasonality. However, life-history and behavioural strategies may also buffer energetic shortages and reduce dependency on environmental cycles. Here, we propose and test an integrative framework integrating climatic, life-history and behavioural factors using high-resolution measures of reproductive seasonality for 132 wild primate populations from 94 species. As expected, reproductive seasonality declines at lower latitudes, in less seasonal and in less predictable environments, even after controlling for productivity. It also decreases in species that spread reproductive costs by extending developmental periods, or when a higher infant mortality urges females to resume fertility shortly after loss. Unexpectedly, reproductive seasonality increases with environmental productivity and is not reduced by cognitive (foraging innovations), social (allomaternal care), or ecological (dietary breadth) buffering. Broader diets even enhance seasonality. These findings suggest that reproductive seasonality emerges from opportunity more than from constraints in productive environments, where females exploit abundant resources to accelerate their reproductive pace. Together, our results shed light on the diverse selective pressures shaping primate reproductive seasonality, including climate, life-history pace, and infanticide risk, and help to explain why humans reproduce year-round.

Chemical sensing via olfaction constitutes a most ancient form of inter-organism communication. But acoustical signaling via tonal and rhythmic patterning is also common among higher vertebrates. Animals that live in well ventilated habitats and move in diasporic ways have further evolved more spectrally varied and discretized call structure. But unlike song in birds, researchers have struggled to locate isolated nucleii specialized for music cognition. The brain stem, midbrain, hindbrain, and forebrain, however, all largely associate with aspects of musical performance, perception, memory, and emotion. I hypothesized that spectral features of musical display evolved as honest signals of spatial cognition for precarious locomotor tasks associated with nurturing and protecting vulnerable offspring. I investigated possible connections between motor, visual, and spatial cognitive areas in relation to both signaler production and receiver processing of acoustical features of musical output. Brain component volume fractions of 42 parts from 48 primates were compiled, from a single source, and compared against a vocal complexity index (ARDI) as well as individual musical feature scores: including tone, interval, repetition, transposition rhythm, and unique syllable count. Structures for spatial and visual perception as well as motor control and emotional processing associated moderately with areas used by species who produce calls with both temporal and spectral musical features. These findings are consistent with a dual (both receiver- and signaler-side) function of musical signals. Associations with spatio-social areas (e.g. schizocortex and insula) support direct selection for a paralimbic-based neighbor orienting [PIANO] sensory modality for mapping and anticipating movement of fellow arboreal cohabitants. Associations with motor areas (e.g. LGN, mid-brain, and thalamus) support the complementary model that signaler capacities for spatio-motive emplacement [ME] are indirectly selected by conspecific receivers. This dual manifestation in low-parity species that locomote in diasporic ways through (arboreally) diffuse habitats, is compatible with musicality serving as courtship signals by long-term mates with consistent and reliable spatial capacities directly relevant to care of vulnerable (arboreal) offspring.

1Mammals exhibit two distinct reproductive strategies: altriciality, where neonates are highly underdeveloped, and precociality, where neonates are well-developed. The neonatal developmental state of deep nodes in mammalian phylogeny remains unresolved. Here, we use phylogenetic comparative methods to reconstruct the evolutionary history of neonatal maturity in mammals and demonstrate that the eutherian ancestor likely gave birth to precocial neonates. This finding contradicts the prevailing view that precociality evolved multiple times within the eutherian lineage. We contextualize this result with three lines of evidence. First, recent fossil evidence suggests that precocial life history traits arose early in therian evolution. Second, altricial eutherian neonates are markedly more developed at birth compared to altricial non-eutherians, suggesting a precocial ancestry in eutherian evolution. Third, reproductive traits that enable prolonged pregnancy originated in the stem lineage prior to the eutherian ancestor. Based on these findings, we propose an alternative model for the evolutionary history of precociality in mammals.

Cannibalism is among the strongest and most widespread food taboos in human societies, yet archaeological, ethnographic, and historical evidence indicates that it has repeatedly emerged across diverse human populations. This coexistence of recurrent practice and persistent prohibition raises a fundamental question: when does cannibalism become adaptive, and why is it typically suppressed? We address this problem using a formal model that treats cannibalism as a potential food source subject to energetic benefits and multiple sources of cost. Nutritional gains are modelled using a saturating function of caloric intake, while costs arise from acquisition, digestion, and infection. Infection costs are represented as a stochastic process whose mean increases with the length of the trophic transmission chain, capturing the risks associated with repeated within-species consumption. Analysing the expected energetic balance across levels of food availability and cannibalism order reveals narrow ecological conditions in which cannibalism yields a positive expected balance and broader conditions in which it is strongly disfavoured. The model provides a framework for interpreting archaeological and ethnographic findings by specifying boundary conditions and identifying the most probable ecological scenarios under which different forms of cannibalism are expected to occur. The results predict that cannibalism is most likely under extreme resource scarcity, when acquisition costs are low and infection risks are constrained, while sustained or high-order cannibalism rapidly becomes unviable due to escalating infection costs. Overall, the findings suggest that cannibalism is best understood as a conditional trade-off rather than a behavioural anomaly, with cultural taboos functioning as adaptive responses to nonlinear epidemiological risks.

Using the voice to produce sound is a widespread form of communication and plays an important role in contexts as diverse as parent-offspring interactions and courtship. Variation in the tempo and mode of vocal signal evolution has been studied in a phylogenetic context within orders or classes, but understanding vocal signal evolution ultimately requires comparison across all major lineages involved. Here we used comparative analyses to investigate the evolution of dominant frequency (i.e., the frequency with the highest energy content) and its association with body weight across 873 species of mammals, birds and frogs. In agreement with previous studies, we found that the negative allometric relationship between body weight and vocal frequency is a general feature of vocal systems. In addition, we found mammals to consistently vocalize at higher frequencies, and evolved their vocalizations at around 6-fold faster rates than those of birds and frogs. Although all three groups strongly rely on vocal communication, our findings show that only mammals have extensively explored the spectral acoustic space. We argue that such high vocal diversity of mammals is made possible by their unique hearing system, which evolved in the context of a small, parental-caring, nocturnal and insectivore ancestor, and has allowed them to detect, and therefore to evolve, a richer array of frequencies than other tetrapods.

Multilevel social systems in birds and mammals have attracted considerable interest, not least because they share some similarities with the natural structural organisation of human societies. I use a fractal analysis of a taxonomically wide range of species reported to have multilevel social systems to show that these in fact involve two very different phenomena: those that are fractally modular and those that are casually modular. The first have a strictly fractal structure identical to that found in human societies; the second lack formal structural coherence and are closer in form to casual herds. The former are associated with larger neocortices than the latter, suggesting that they may be cognitively more demanding. Understanding the evolution of multilevel systems and the cognition that underpins them obliges us to adopt a more nuanced approach to social evolution.

Studying the prevalence of putatively rare behaviours, such as tool use, is challenging because absence of evidence can arise either from a species inability to produce the behaviour or from insufficient research effort. Here, we tackle this challenge by combining crowdsourcing and phylogenetic modelling to approximate actual rates of a rarely observed behaviour based on limited data, targeting tool use in parrots. Crowdsourcing on a social media platform revealed novel instances of tool use in 17 parrot species, more than doubling the confirmed number of tool-using parrot species from 11 (3%) to 28 (7%). Phylogenetic modelling ranked additional species that are most likely to be unobserved tool users, suggesting that between 11% and 17% of extant parrot species may be tool users. These discoveries have implications for inferences about the evolutionary drivers and origins of tool use in parrots, revealing associations with relative brain size and feeding generalism and indicating several genera where tool use was likely an ancestral trait. Overall, our findings challenge the assumption that current sampling effort captures the full distribution of putatively rare animal behaviours. Combining our sampling and analysis methods offers a fruitful approach for investigating the distribution, drivers, and origins of other rare behaviours. This working paper has not yet been peer-reviewed.

Natural selection widely favours the largest within animal species. Why body sizes are declining in the worlds temperate birds is therefore mechanistically confusing and ecologically worrying. We argue that understanding the causes of these declines requires knowledge of how complete, body mass probability distributions - not just averages - are moving. Using data from 159 North American bird species - spanning 26 families, 53{degrees} of latitude, and 25 years - we show that body mass distributions are not only downgrading, but also narrowing, and losing their upper tails (the heaviest individuals), with the largest changes occurring at southern range limits. Combining fitness models with a novel, distributional Price equation revealed that these changes are increasingly driven by phenotypic plasticity, not selection or genetic drift, and may yet be reversible.

As humans increasingly modify the natural world, many animals have responded by changing their behaviour. Predicting the extent of these responses is a key step in conserving these species. For example, the tendency for some species of birds to incorporate anthropogenic items - particularly plastic material - into their nests is of increasing concern, as in some cases this behaviour has harmful effects on both adults and young. Studies of this phenomenon, however, have to date been limited in geographic and taxonomic scope. To investigate the global correlates of anthropogenic (including plastic) nest material use, we used Bayesian phylogenetic mixed models and a dataset of recorded nest materials in 6,147 species of birds. We find that after controlling for research effort, anthropogenic nest material use is correlated with proximity to human landscape modification, synanthropic (artificial) nesting locations, breeding environment, and the number of materials that has been recorded within the species nest. We also demonstrate that anthropogenic nest material use is unrelated to body mass, range size, or conservation status. These results indicate that anthropogenic materials are more likely to be included in nests when they are more readily available, as well as potentially by species who have more flexibility in nest material choice.