Gustavo Burin’s research while affiliated with Natural History Museum, London and other places

The fossil record of true seals (Family Phocidae) is mostly made up of isolated bones, some of which are type specimens. Previous studies have sought to increase referral of non-overlapping and unrelated fossils to these taxa using the 'Ecomorphotype Hypothesis', which stipulates that certain differences in morphology between taxa represent adaptations to differing ecology. On this basis, bulk fossil material could be lumped to a specific ecomorphotype, and then referred to species in that ecomorphotype, even if they are different bones. This qualitative and subjective method has been used often to expand the taxonomy of fossil phocids, but has never been quantitatively tested. We test the proposed ecomorphotypes using morphometric analysis of fossil and extant northern true seal limb bones, specifically principal components analysis and discriminant function analysis. A large amount of morphological overlap between ecomorphotypes, and poor discrimination between them, suggests that the 'Ecomorphotype Hypothesis' is not a valid approach. Further, the analysis failed to assign fossils to ecomorphotypes designated in previous studies, with some fossils from the same taxa being designated as different ecomorphotypes. The failure of this approach suggests that all fossils referred using this method should be considered to have unknown taxonomic status. In light of this, and previous findings that phocid limb bones have limited utility as type specimens, we revise the status of named fossil phocid species. We conclude that the majority of named fossil phocid taxa should be considered nomina dubia. Subjects Paleontology, Taxonomy

Pinnipeds (seals, sea lions, walruses, and their fossil relatives) are one of the most successful mammalian clades to live in the oceans. Despite a well-resolved molecular phylogeny and a global fossil record, a complete understanding of their macroevolutionary dynamics remains hampered by a lack of formal analyses that combine these 2 rich sources of information. We used a meta-analytic approach to infer the most densely sampled pinniped phylogeny to date (36 recent and 93 fossil taxa) and used phylogenetic paleobiological methods to study their diversification dynamics and biogeographic history. Pinnipeds mostly diversified at constant rates. Walruses, however, experienced rapid turnover in which extinction rates ultimately exceeded speciation rates from 12 to 6 Ma, possibly due to changing sea levels and/or competition with otariids (eared seals). Historical biogeographic analyses, including fossil data, allowed us to confidently identify the North Pacific and the North Atlantic (plus or minus Paratethys) as the ancestral ranges of Otarioidea (eared seals + walrus) and crown phocids (earless seals), respectively. Yet, despite the novel addition of stem pan-pinniped taxa, the region of origin for Pan-Pinnipedia remained ambiguous. These results suggest further avenues of study in pinnipeds and provide a framework for investigating other groups with substantial extinct and extant diversity.

Mutualisms have driven the evolution of extraordinary structures and behavioural traits, but their impact on traits beyond those directly involved in the interaction remains unclear. We addressed this gap using a highly evolutionarily replicated system – epiphytes in the Rubiaceae forming symbioses with ants. We employed models that allow us to test the influence of discrete mutualistic traits on continuous non‐mutualistic traits. Our findings are consistent with mutualism shaping the pace of morphological evolution, strength of selection and long‐term mean of non‐mutualistic traits in function of mutualistic dependency. While specialised and obligate mutualisms are associated with slower trait change, less intimate, facultative and generalist mutualistic interactions – which are the most common – have a greater impact on non‐mutualistic trait evolution. These results challenge the prevailing notion that mutualisms solely affect the evolution of interaction‐related traits via stabilizing selection and instead demonstrate a broader role for mutualisms in shaping trait evolution.

Composite traits involve multiple components that, only when combined, gain a new synergistic function. Thus, how they evolve remains a puzzle. We combined field experiments, microscopy, chemical analyses, and laser Doppler vibrometry with comparative phylogenetic analyses to show that two carnivorous Nepenthes pitcher plant species independently evolved similar adaptations in three distinct traits to acquire a new, composite trapping mechanism. Comparative analyses suggest that this new trait arose convergently through “spontaneous coincidence” of the required trait combination, rather than directional selection in the component traits. Our results indicate a plausible mechanism for composite trait evolution and highlight the importance of stochastic phenotypic variation as a facilitator of evolutionary novelty.

Adaptive landscapes are central to evolutionary theory, forming a conceptual bridge between micro- and macroevolution.1,2,3,4 Evolution by natural selection across an adaptive landscape should drive lineages toward fitness peaks, shaping the distribution of phenotypic variation within and among clades over evolutionary timescales.5 The location and breadth of these peaks in phenotypic space can also evolve,4 but whether phylogenetic comparative methods can detect such patterns has largely remained unexplored.6 Here, we characterize the global and local adaptive landscape for total body length in cetaceans (whales, dolphins, and relatives), a trait that spans 5 orders of magnitude, across their ∼53 million year evolutionary history. Using phylogenetic comparative methods, we analyze shifts in long-term mean body length7 and directional changes in average trait values8 for 345 living and fossil cetacean taxa. Remarkably, we find that the global macroevolutionary adaptive landscape of cetacean body length is relatively flat, with very few peak shifts occurring after cetaceans entered the oceans. Local peaks are more numerous and manifest as trends along branches linked to specific adaptations. These results contrast with previous studies using only extant taxa,9 highlighting the vital role of fossil data for understanding macroevolution.10,11,12 Our results indicate that adaptive peaks are dynamic and are associated with subzones of local adaptations, creating moving targets for species adaptation. In addition, we identify limits in our ability to detect some evolutionary patterns and processes and suggest that multiple approaches are required to characterize complex hierarchical patterns of adaptation in deep time.

Adaptive landscapes are central to evolutionary theory, forming a conceptual bridge between micro- and macro-evolution. Evolution by natural selection across an adaptive landscape should drive lineages towards fitness peaks, shaping the distribution of phenotypic variation within and among clades over evolutionary timescales. Constant shifts in selection pressures mean the peaks themselves also evolve through time, thus a key challenge is to identify these "ghosts of selection past". Here, we characterise the global and local adaptive landscape for total length in cetaceans (whales and dolphins) across their approx. 53 million year evolutionary history, using 345 living and fossil taxa. We analyse shifts in long-term mean size and directional changes in average trait values using cutting-edge phylogenetic comparative methods. We demonstrate that the global macroevolutionary adaptive landscape of cetacean body size is relatively flat, with very few peak shifts after cetaceans colonised the oceans. Local peaks represent trends along branches linked to specific adaptations such as deep diving. These results contrast with previous studies using only extant taxa, highlighting the vital role of fossil data for understanding macroevolutionary dynamics. Our results indicate that adaptive peaks are constantly changing and are associated with subzones of local adaptations, resembling turbulent waters with waves and ripples, creating moving targets for species adaptation. In addition, we identify limits in our ability to detect some evolutionary patterns and processes, and suggest multiple approaches are required to characterise complex hierarchical patterns of adaptation in deep-time.

Body size and shape play fundamental roles in organismal function and it is expected that animals may possess body proportions that are well-suited to their ecological niche. Tetrapods exhibit a diverse array of body shapes, but to date this diversity in body proportions and its relationship to ecology have not been systematically quantified. Using whole-body skeletal models of 410 extinct and extant tetrapods, we show that allometric relationships vary across individual body segments thereby yielding changes in overall body shape as size increases. However, we also find statistical support for quadratic relationships indicative of differential scaling in small-medium versus large animals. Comparisons of locomotor and dietary groups highlight key differences in body proportions that may mechanistically underlie occupation of major ecological niches. Our results emphasise the pivotal role of body proportions in the broad-scale ecological diversity of tetrapods.

Natricine snakes are geographically widespread, species rich (with ~250 extant species) and both morphologically and ecologically diverse. We present a multilocus DNA sequence phylogeny for 249 natricine specimens representing 189 named species, including 69 specimens and 21 species not previously sampled. Our inferred Bayesian and maximum likelihood trees form the basis for evaluations of genus-level classification, historical biogeography, lineage diversification, and dietary, habit and reproductive-mode diversity and evolution, although several, mostly deeper, relationships remain poorly resolved. The optimal trees support natricine origins in Asia, with dispersals to Australo-Melanesia, sub-Saharan Africa (including Seychelles Archipelago, excluding Aldabra), Europe and North Africa and into North and Central America. Viviparity appears to have evolved independently three times in Natricinae but was not significantly associated with an aquatic habit. We found limited associations between habit and diet categories. We propose generic reallocations for four natricine species and highlight other points of uncertainty in natricine classification.

The evolution of ecological networks Plants and the animals that eat their fruits and disperse their seeds form complex networks of mutualistic interactions. The structures of many such networks and the ecological forces that shape them are well known, but their deeper evolutionary history has received little attention. Burin et al. address this knowledge gap in a study of frugivorious bird species in documented seed-dispersal networks around the world (see the Perspective by Bello and Barreto). Species occupying central positions in frugivory networks, which thus interact with many plant species, tend to belong to lineages that are more stable over macroevolutionary time scales. These patterns are more evident in regions with warmer and wetter climates and provide evidence that evolutionary processes can leave a signal on the structure of current ecological networks. Science , this issue p. 733 see also p. 682