A quantitative test of the "Ecomorphotype Hypothesis" for fossil true seals (Family Phocidae).

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.

Charting the course of pinniped evolution: insights from molecular phylogeny and fossil record integration.

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 drive plant trait evolution beyond interaction-related traits.

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.

Convergence in carnivorous pitcher plants reveals a mechanism for composite 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.

The dynamic adaptive landscape of cetacean body size.

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 an order 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.

Body size, shape and ecology in tetrapods.

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.

Macroevolutionary stability predicts interaction patterns of species in seed dispersal networks.

Assessing deep-time mechanisms affecting the assembly of ecological networks is key to understanding biodiversity changes on broader time scales. We combined analyses of diversification rates with interaction network descriptors from 468 bird species belonging to 29 seed dispersal networks to show that bird species that contribute most to the network structure of plant-frugivore interactions belong to lineages that show higher macroevolutionary stability. This association is stronger in warmer, wetter, less seasonal environments. We infer that the macroevolutionary sorting mechanism acts through the regional pool of species by sorting species on the basis of the available relative differences in diversification rates, rather than absolute rates. Our results illustrate how the interplay between interaction patterns and diversification dynamics may shape the organization and long-term dynamics of ecological networks.

How Well Can We Estimate Diversity Dynamics for Clades in Diversity Decline?

The fossil record shows that the vast majority of all species that ever existed are extinct and that most lineages go through an expansion and decline in diversity. However, macroevolutionary analyses based upon molecular phylogenies have difficulty inferring extinction dynamics, raising questions about whether the neontological record can contribute to an understanding of the decline phenomenon. Two recently developed diversification methods for molecular phylogenies (RPANDA and BAMM) incorporate models that theoretically have the capacity to capture decline dynamics by allowing extinction to be higher than speciation. However, the performance of these frameworks over a wide range of decline scenarios has not been studied. Here, we investigate the behavior of these methods under decline scenarios caused by decreasing speciation and increasing extinction through time on simulated trees at fixed intervals over diversity trajectories with expansion and decline phases. We also compared method performance over a comprehensive data set of 214 empirical trees. Our results show that both methods perform equally well when varying speciation rates control decline. When decline was only caused by an increase in extinction rates both methods wrongly assign the variation in net diversification to a drop in speciation, even though the positive gamma values of those trees would suggest otherwise. We also found a tendency for RPANDA to favor increasing extinction and BAMM to favor decreasing speciation as the most common cause of decline in empirical trees. Overall our results shed light on the limitations of both methods, encouraging researchers to carefully interpret the results from diversification studies.

Arboreality constrains morphological evolution but not species diversification in vipers.

An increase in ecological opportunities, either through changes in the environment or acquisition of new traits, is frequently associated with an increase in species and morphological diversification. However, it is possible that certain ecological settings might prevent lineages from diversifying. Arboreality evolved multiple times in vipers, making them ideal organisms for exploring how potentially new ecological opportunities affect their morphology and speciation regimes. Arboreal snakes are frequently suggested to have a very specialized morphology, and being too large, too small, too heavy, or having short tails might be challenging for them. Using trait-evolution models, we show that arboreal vipers are evolving towards intermediate body sizes, with longer tails and more slender bodies than terrestrial vipers. Arboreality strongly constrains body size and circumference evolution in vipers, while terrestrial lineages are evolving towards a broader range of morphological variants. Trait-dependent diversification models, however, suggest similar speciation rates between microhabitats. Thus, we show that arboreality might constrain morphological evolution but not necessarily affect the rates at which lineages generate new species.

Omnivory in birds is a macroevolutionary sink.

Diet is commonly assumed to affect the evolution of species, but few studies have directly tested its effect at macroevolutionary scales. Here we use Bayesian models of trait-dependent diversification and a comprehensive dietary database of all birds worldwide to assess speciation and extinction dynamics of avian dietary guilds (carnivores, frugivores, granivores, herbivores, insectivores, nectarivores, omnivores and piscivores). Our results suggest that omnivory is associated with higher extinction rates and lower speciation rates than other guilds, and that overall net diversification is negative. Trait-dependent models, dietary similarity and network analyses show that transitions into omnivory occur at higher rates than into any other guild. We suggest that omnivory acts as macroevolutionary sink, where its ephemeral nature is retrieved through transitions from other guilds rather than from omnivore speciation. We propose that these dynamics result from competition within and among dietary guilds, influenced by the deep-time availability and predictability of food resources.