Phylogenetic comparative investigations of sexual selection and cognitive evolution in primates

A full understanding of any biological trait requires investigation of its evolutionary origin. Primates inspire great curiosity amongst researchers due to the remarkable diversity across species in both anatomical and behavioural traits, including sociality, sexual behaviour, life histories, neuro-anatomy, cognitive abilities and behavioural repertoires. The study of primates has involved comparative approaches since its inception, however, the necessary tools for statistically investigating the macro-evolutionary processes responsible for current diversity in biological traits have been developed only in the last 30 years or so, namely phylogenetic reconstruction and phylogenetic comparative methods. Amongst a multitude of evolutionary questions that can be addressed by phylogenetic comparative analyses, this thesis attempts to address two in particular, concerning primates. First, chapters 3 and 4 use meta-analysis and phylogenetic comparative analyses to investigate the evolution of large, brightly coloured ‘exaggerated sexual swellings’ in female Catarrhine (‘Old World’) primates. Together, chapters 3 and 4 show that such swellings are signals of temporal fertility, and present evidence to suggest that swellings co-evolved with conditions favouring male mate choice and cryptic female choice, therefore shedding light on the general conditions under which female signals of temporal fertility should evolve. Second, chapters 5 and 6 use phylogenetic comparative analyses investigate the evolution of enlarged brain size in the primate order. Together, chapters 5 and 6 suggest that multiple selection pressures have contributed to diversity in brain size and cognitive traits across primates, including sociality, intra-sexual competition and extended life history. Further, analyses presented in chapter 6 suggest that reliance on learned behaviour is a self-reinforcing evolutionary process, favouring ‘runaway’ increases in cognitive abilities and reliance on culture in some primate lineages, which parallels increases in brain size, cognitive ability and reliance on culture in human evolution

Maternal investment, life histories, and the evolution of brain structure in primates

Life history is a robust correlate of relative brain size: larger-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. The cognitive buffer hypothesis (CBH) proposes an adaptive explanation for this relationship: large brains may permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing for reduced mortality and increased lifespan. By contrast, the developmental costs hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains, predicting correlations with pre-adult life-history phases. Here, we test novel predictions of the hypotheses in primates applied to the neocortex and cerebellum, two major brain structures with distinct developmental trajectories. While neocortical growth is allocated primarily to pre-natal development, the cerebellum exhibits relatively substantial post-natal growth. Consistent with the DCH, neocortical expansion is related primarily to extended gestation while cerebellar expansion to extended post-natal development, particularly the juvenile period. Contrary to the CBH, adult lifespan explains relatively little variance in the whole brain or neocortex volume once pre-adult life-history phases are accounted for. Only the cerebellum shows a relationship with lifespan after accounting for developmental periods. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental phases, and imply that environmental input during post-natal maturation may be particularly crucial for the development of cerebellar function. They also suggest that relatively extended post-natal maturation times provide a developmental mechanism for the marked expansion of the cerebellum in the apes

Convergent evolution of elaborate nests as structural defences in birds

The pendent nests of some weaverbird and icterid species are among the most complex structures built by any animal, but why they have evolved remains to be explained. The precarious attachments and extended entrance tunnels characteristic of these nests are widely speculated to act as structural defences against invasion by nest predators, particularly tree-climbing snakes, but this hypothesis has yet to be systematically tested. We use phylogenetic comparative methods to investigate the relationship between nest structure and developmental period length, a proxy for offspring mortality, in weaverbirds (Ploceidae) and icterids (Icteridae), two bird families in which highly elaborate pendent nests have independently evolved. We find that more elaborate nests, particularly those with entrance tunnels, are associated with longer developmental periods in both families. This finding is robust to potentially confounding effects of body mass, phylogenetic relationships, nest location and latitude. Our results are consistent with the hypothesis that elaborate nest structures in birds can function as structural defences, resulting in lower offspring mortality and slower development. More generally, our findings suggest that constructing complex, protective structures may buffer against environmental hazards, reducing extrinsic mortality and contributing to the evolution of slower life histories in diverse animal lineages, even humans

The coevolution of innovation and technical intelligence in primates

In birds and primates, the frequency of behavioural innovation has been shown to covary with absolute and relative brain size, leading to the suggestion that large brains allow animals to innovate, and/or that selection for innovativeness, together with social learning, may have driven brain enlargement. We examined the relationship between primate brain size and both technical (i.e. tool using) and non-technical innovation, deploying a combination of phylogenetically informed regression and exploratory causal graph analyses. Regression analyses revealed that absolute and relative brain size correlated positively with technical innovation, and exhibited consistently weaker, but still positive, relationships with non-technical innovation. These findings mirror similar results in birds. Our exploratory causal graph analyses suggested that technical innovation shares strong direct relationships with brain size, body size, social learning rate and social group size, whereas non-technical innovation did not exhibit a direct relationship with brain size. Nonetheless, non-technical innovation was linked to brain size indirectly via diet and life-history variables. Our findings support ‘technical intelligence’ hypotheses in linking technical innovation to encephalization in the restricted set of primate lineages where technical innovation has been reported. Our findings also provide support for a broad co-evolving complex of brain, behaviour, life-history, social and dietary variables, providing secondary support for social and ecological intelligence hypotheses. The ability to gain access to difficult-to-extract, but potentially nutrient-rich, resources through tool use may have conferred on some primates adaptive advantages, leading to selection for brain circuitry that underlies technical proficiency.PostprintPeer reviewe

The evolutionary drivers of primate scleral coloration

The drivers of divergent scleral morphologies in primates are currently unclear, though white sclerae are often assumed to underlie human hyper-cooperative behaviours. Humans are unusual in possessing depigmented sclerae whereas many other extant primates, including the closely-related chimpanzee, possess dark scleral pigment. Here, we use phylogenetic generalized least squares (PGLS) analyses with previously generated species-level scores of proactive prosociality, social tolerance (both n = 15 primate species), and conspecific lethal aggression (n = 108 primate species) to provide the first quantitative, comparative test of three existing hypotheses. The ‘self-domestication’ and ‘cooperative eye’ explanations predict white sclerae to be associated with cooperative, rather than competitive, environments. The ‘gaze camouflage’ hypothesis predicts that dark scleral pigment functions as gaze direction camouflage in competitive social environments. Notably, the experimental evidence that non-human primates draw social information from conspecific eye movements is unclear, with the latter two hypotheses having recently been challenged. Here, we show that white sclerae in primates are associated with increased cooperative behaviours whereas dark sclerae are associated with reduced cooperative behaviours and increased conspecific lethal violence. These results are consistent with all three hypotheses of scleral evolution, suggesting that primate scleral morphologies evolve in relation to variation in social environment

Beak shape and nest material use in birds

This work was supported by a BBSRC Discovery Fellowship (grant no. BB/S01019X/1); the John Templeton Foundation (grant no. 60501); and the European Research Council (grant no. 788203).The evolution of behaviour can both influence, and be influenced by, morphology. Recent advances in methods and data availability have facilitated broad-scale investigations of physical form and behavioural function in many contexts, but the relationship between animal morphology and object manipulation-particularly objects used in construction-remains largely unknown. Here, we employ a new global database of nest materials used by 5924 species of birds together with phylogenetically informed random forest models to evaluate the link between beak shape and these nest-building materials. We find that beak morphology, together with species diet and access to materials, can predict nest-material use above chance and with high accuracy (68-97%). Much of this relationship, however, is driven by phylogenetic signal and sampling biases. We therefore conclude that while variation in nest material use is linked with that of beak shape across bird species, these correlations are modulated by the ecological context and evolutionary history of these species.Publisher PDFPeer reviewe

Anthropogenic nest material use in a global sample of birds

As humans increasingly modify the natural world, many animals have responded by changing their behaviour. Understanding and 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 adults, young and eggs. Studies of this phenomenon, however, have to date been largely 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 data set of recorded nest materials in 6147 species of birds. We find that, after controlling for research effort and proximity to human landscape modifications, anthropogenic nest material use is correlated with synanthropic (artificial) nesting locations, breeding environment and the number of different nest materials the species has been recorded to use. We also demonstrate that body mass, range size, conservation status and brain size do not explain variation in the recorded use of anthropogenic nest materials. 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 that are more flexible in their nest material choice

Nest traits for the world's birds

Funding: H2020 European Research Council, Grant/Award Number: 788203; John Templeton Foundation, Grant/Award Number: 60501.Motivation: A well-constructed nest is a key element of successful reproduction in most species of birds, and nest morphology varies widely across the class. Macroecological and macroevolutionary studies tend to group nest design into a small number of discrete categories, often based on taxonomic inference. In reality, however, many species display considerable intraspecific variation in their nest-building behaviour, and broad-level categories may include several functionally distinct nest types. To address this imprecision in the literature and facilitate future studies of broad-scale variation in avian parental care, we here introduce a detailed, global comparative database of nest building in birds, together with preliminary correlations between these traits and species-level environmental variables. Main types of variables contained: We present species-level data for nest structure, location, height, material composition, sex of builder, building time and nest dimensions. Spatial location and grain: Global. Maps are presented at the 10 × 10 level. Time period and grain: Included species are generally extant, although we present some data for recently extinct taxa. The data were collected in 2017–2021 and was drawn from secondary sources published in 1992–2021. Major taxa and level of measurement: Partial or complete trait data is presented for 8601 species of birds, representing 36 of 36 orders and 239 of 243 families. Software format: Data have been uploaded as Supplementary Material in .csv format and are separated by species and source for all traits (Dataset S1, and Metadata) as well as summarized at the species level for the major structure and location variables (Dataset S2, and Metadata).Publisher PDFPeer reviewe

Nest traits for the world's birds

We thank Mike Hansell, Mike Benton and members of the Healy and Lala labs, especially Sophie Edwards and Helen Spence-Jones, for comments on project design. This work was funded by the John Templeton Foundation (#60501 to KNL) and the European Research Council (788203 ‘Innovation’).Peer reviewe