Macroevolutionary Patterns Research Articles

Convergence in sympatric swallowtail butterflies reveals ecological interactions as a key driver of worldwide trait diversification

Ecological interactions can promote phenotypic diversification in sympatric species. While competition can enhance trait divergence, other ecological interactions may promote convergence in sympatric species. Within butterflies, evolutionary convergences in wing color patterns have been reported between distantly related species, especially in females of palatable species, where mimetic color patterns are promoted by predator communities shared with defended species living in sympatry. Wing color patterns are also often involved in species recognition in butterflies, and divergence in this trait has been reported in closely related species living in sympatry as a result of reproductive character displacement. Here, we investigate the effect of sympatry between species on the convergence vs. divergence of their wing color patterns in relation to phylogenetic distance, focusing on the iconic swallowtail butterflies (family Papilionidae). We developed an unsupervised machine learning-based method to estimate phenotypic distances among wing color patterns of 337 species, enabling us to finely quantify morphological diversity at the global scale among species and allowing us to compute pairwise phenotypic distances between sympatric and allopatric species pairs. We found phenotypic convergence in sympatry, stronger among distantly related species, while divergence was weaker and restricted to closely related males. The convergence was stronger among females than males, suggesting that differential selective pressures acting on the two sexes drove sexual dimorphism. Our results highlight the significant effect of ecological interactions driven by predation pressures on trait diversification in Papilionidae and provide evidence for the interaction between phylogenetic proximity and ecological interactions in sympatry, acting on macroevolutionary patterns of phenotypic diversification.

Increased hydraulic risk in assemblages of woody plant species predicts spatial patterns of drought-induced mortality

Predicting drought-induced mortality (DIM) of woody plants remains a key research challenge under climate change. Here, we integrate information on the edaphoclimatic niches, phylogeny and hydraulic traits of species to model the hydraulic risk of woody plants globally. We combine these models with species distribution records to estimate the hydraulic risk faced by local woody plant species assemblages. Thus, we produce global maps of hydraulic risk and test for its relationship with observed DIM. Our results show that local assemblages modelled as having higher hydraulic risk present a higher probability of DIM. Metrics characterizing this hydraulic risk improve DIM predictions globally, relative to models accounting only for edaphoclimatic predictors or broad functional groupings. The methodology we present here allows mapping of functional trait distributions and elucidation of global macro-evolutionary and biogeographical patterns, improving our ability to predict potential global change impacts on vegetation.

Adaptive immune response selects for postponed maturation and increased body size

Abstract The Major Histocompatibility Complex (MHC) genes encode proteins that initiate the adaptive immune response by presenting pathogen‐derived antigenic peptides to T lymphocytes. Host–pathogen coevolution drives MHC polymorphism, introducing intraspecific variation in host life expectancy. This variation interacts with optimal growth strategy, as growth increases reproductive potential. While mortality rate and body size‐dependent fecundity are major factors shaping life histories, the effect of intraspecific variation in MHC‐based immunity on the evolution of growth strategies and host body size remains unknown. Here, we model how host MHC–pathogen coevolution—and its concomitant impact on host mortality—can affect the evolution of host life histories, as represented by age at maturation and body size. Life histories were compared in scenarios with and without adaptive immune response under equal population‐level mortality rates. We show that host–pathogen coevolutionary dynamics selects for postponed maturation and increased body size. Although MHC genes and genes that determine body size were physically unlinked, selection imposed by the Red Queen process generated linkage disequilibrium between immunocompetent MHC alleles and the maturation‐postponing alleles that prolong growth phase and increase body size. Particularly large body size was attained when pathogens mutated slowly, thus allowing the advantage of resistant MHC alleles to persist over multiple generations. The emergence of adaptive immunity, which is pathogen‐specific and enables immunological memory, is considered a major evolutionary innovation of vertebrates. Our work suggests that the adaptive immune response, mediated by polymorphic MHC genes, may drive the evolution of host body size. This form of adaptive immunity may have thus predisposed vertebrates to evolve large body size and exhibit the macroevolutionary patterns of increasing body size over time that have been detected in comparative studies. Read the free Plain Language Summary for this article on the Journal blog.

Macroevolutionary patterns in the pelvis, stylopodium and zeugopodium of megalosauroid theropod dinosaurs and their importance for locomotor function.

During the Mesozoic, non-avian theropods represented one of the most successful clades globally distributed, with a wide diversity of forms. An example is the clade Megalosauroidea, which included medium- to large-bodied forms. Here, we analyse the macroevolution of the locomotor system in early Theropoda, emphasizing the Megalosauroidea. We scored the Spinosaurus neotype in a published taxon-character matrix and described the associated modifications in character states, mapping them onto a phylogeny and using these to study disparity. In the evolution of Megalosauroidea, there was the mosaic emergence of a low swollen ridge; enlargement of the posterior brevis fossa and emergence of a posterodorsal process on the ilium in some megalosauroids; emergence of a femoral head oriented anteromedially and medially angled, and appearance of posterolaterally oriented medial femoral condyles in spinosaurids. The greatest morphological disparity is in the ilium of megalosaurids; the ischium seems to have a high degree of homoplasy; there is a clear distinction in the femoral morphospace regarding megalosauroids and other theropods; piatnitzkysaurids show considerable disparity of zeugopodial characters. These reconstructions of osteological evolution form a stronger basis on which other studies could build, such as mapping of pelvic/appendicular musculature and/or correlating skeletal traits with changes in locomotor function.

Effect of Plant Defenses and Plant Nutrients on the Performance of Specialist and Generalist Herbivores of Datura: A Macroevolutionary Study.

Macroevolutionary patterns in the association between plant species and their herbivores result from ecological divergence promoted by, among other factors, plants' defenses and nutritional quality, and herbivore adaptations. Here, we assessed the performance of the herbivores Lema trilineata daturaphila, a trophic specialist on Datura, and Spodoptera frugiperda, a polyphagous pest herbivore, when fed with species of Datura. We used comparative phylogenetics and multivariate methods to examine the effects of Datura species' tropane alkaloids, leaf trichomes, and plant macronutrients on the two herbivores´ performances (amount of food consumed, number of damaged leaves, larval biomass increment, and larval growth efficiency). The results indicate that species of Datura do vary in their general suitability as food host for the two herbivores. Overall, the specialist performs better than the generalist herbivore across Datura species, and performance of both herbivores is associated with suites of plant defenses and nutrient characteristics. Leaf trichomes and major alkaloids of the Datura species are strongly related to herbivores' food consumption and biomass increase. Although hyoscyamine better predicts the key components of the performance of the specialist herbivore, scopolamine better predicts the performance of the generalist; however, only leaf trichomes are implicated in most performance components of the two herbivores. Nutrient quality more widely predicts the performance of the generalist herbivore. The contrasting effects of plant traits and the performances of herbivores could be related to adaptive differences to cope with plant toxins and achieve nutrient balance and evolutionary trade-offs and synergisms between plant traits to deal with a diverse community of herbivores.

The evolutionary origin of the durophagous pelagic stingray ecomorph.

Studies of the origin of evolutionary novelties (novel traits, feeding modes, behaviours, ecological niches, etc.) have considered a number of taxa experimenting with new body plans, allowing them to occupy new habitats and exploit new trophic resources. In the marine realm, colonization of pelagic environments by marine fishes occurred recurrently through time. Stingrays (Myliobatiformes) are a diverse clade of batoid fishes commonly known to possess venomous tail stings. Current hypotheses suggest that stingrays experimented with a transition from a benthic to a pelagic/benthopelagic habitat coupled with a transition from a non-durophagous diet to extreme durophagy. However, there is no study detailing macroevolutionary patterns to understand how and when habitat shift and feeding specialization arose along their evolutionary history. A new exquisitely preserved fossil stingray from the Eocene Konservat-Lagerstätte of Bolca (Italy) exhibits a unique mosaic of plesiomorphic features of the rajobenthic ecomorph, and derived traits of aquilopelagic taxa, that helps to clarify the evolutionary origin of durophagy and pelagic lifestyle in stingrays. A scenario of early evolution of the aquilopelagic ecomorph is proposed based on new data, and the possible adaptive meaning of the observed evolutionary changes is discussed. The body plan of †Dasyomyliobatis thomyorkei gen. et sp. nov. is intermediate between the rajobenthic and more derived aquilopelagic stingrays, supporting its stem phylogenetic position and the hypothesis that the aquilopelagic body plan arose in association with the evolution of durophagy and pelagic lifestyle from a benthic, soft-prey feeder ancestor.

Speciation and development.

Understanding general principles about the origin of species remains one of the foundational challenges in evolutionary biology. The genomic divergence between groups of individuals can spawn hybrid inviability and hybrid sterility, which presents a tantalizing developmental problem. Divergent developmental programs may yield either conserved or divergent phenotypes relative to ancestral traits, both of which can be responsible for reproductive isolation during the speciation process. The genetic mechanisms of developmental evolution involve cis- and trans-acting gene regulatory change, protein-protein interactions, genetic network structures, dosage, and epigenetic regulation, all of which also have roots in population genetic and molecular evolutionary processes. Toward the goal of demystifying Darwin's "mystery of mysteries," this review integrates microevolutionary concepts of genetic change with principles of organismal development, establishing explicit links between population genetic process and developmental mechanisms in the production of macroevolutionary pattern. This integration aims to establish a more unified view of speciation that binds process and mechanism.

Developmental origin underlies evolutionary rate variation across the placental skull.

The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull's major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

Vegetation dynamics in the Early–Middle Pennsylvanian coal swamps of the Nord-Pas-de-Calais Coalfield, France

During recent years, different studies have focused on characterising plant diversities in the Carboniferous environments of the Variscan Foreland. One of these areas, the Nord-Pas-de-Calais Coalfield, has a Namurian–Westphalian sequence that has historically yielded abundant evidence of vegetation change, but to date, little attention has been paid to its macrofloral diversity dynamics. Here we show, for the first time, a comprehensive characterisation of the diversity changes and macroevolutionary patterns from this coalfield. The results show evidence of low levels of species richness during the Namurian, followed by an exponential diversification at the base of Westphalian. Duckmantian–Bolsovian species diversity continues to progressively increase, suggesting relatively stable conditions at that time. Maximum species richness is observed at the mid-Bolsovian followed by a major depletion during the Asturian. Overall, this pattern is quite similar to that seen in other parts of the Variscan Foreland. However, we see Nord-Pas-de-Calais vegetation diversified earlier than those in the British parts, probably because the dynamics of marine incursions and lacustrine conditions delayed its development in the latter areas. Furthermore, we also see the Asturian decline of the Nord-Pas-de-Calais coal swamp occurred later than in other basins, such as in the Pennines, Ruhr, and South Wales. This scenario suggests that the collapse of this biome was probably caused by increased sediment influx and reduced subsidence, resulting from the northwards migration of the Variscan Mountains. This further supports other studies in Europe advocating that climate change was at most only a subsidiary factor in the collapse of the Pennsylvanian coal swamp biomes.

How do tree density and body size influence acoustic signals in Amazonian nurse frogs?

ABSTRACT The Acoustic Adaptation Hypothesis (AAH) predicts that acoustic signals emitted at sites with greater vegetation density should have spectral and temporal characteristics that increase signal transmission, but there is a pleiotropism related to body size: large animals produce signals with lower frequency. We used 238 advertisement calls of 34 populations of Amazonian nurse frogs from two Amazonian rainforests with different vegetation density to test if tree density influences the evolution of acoustic parameters. We used PGLS to test for relationships between acoustic traits and phenotypic, environmental and geographic predictors. Spectral and temporal features of calls have an allometric relationship with body size. We found a novel quadratic relationship between note duration and body size. The allometric relationship between dominant frequency and body size and a direct effect of tree density indicates that the evolutionary trajectories of Amazonian nurse frogs follow a general macro-evolutionary pattern as in birds. The temporal features of calls have opposite evolutionary trajectories to those predicted by AAH; frogs from lower tree density environments emit longer notes and have higher note rates than those from denser-tree environments. Subtle differences between Amazonian forest types can drive acoustic diversification of temporal and spectral features of calls at micro-evolutionary scales.

Phylogenomics sheds new light on the drivers behind a long-lasting systematic riddle: the figwort family Scrophulariaceae.

The figwort family, Scrophulariaceae, comprises c.2000 species whose evolutionary relationships at the tribal level have proven difficult to resolve, hindering our ability to understand their origin and diversification. We designed a specific probe kit for Scrophulariaceae, targeting 849 nuclear loci and obtaining plastid regions as by-products. We sampled c.87% of the genera described in the family and use the nuclear dataset to estimate evolutionary relationships, timing of diversification, and biogeographic patterns. Ten tribes, including two new tribes, Androyeae and Camptolomeae, are supported, and the phylogenetic positions of Androya, Camptoloma, and Phygelius are unveiled. Our study reveals a major diversification at c.60 million yr ago in some Gondwanan landmasses, where two different lineages diversified, one of which gave rise to nearly 81% of extant species. ASouthern African origin is estimated for most modern-day tribes, with two exceptions, the American Leucophylleae, and the mainly Australian Myoporeae. The rapid mid-Eocene diversification is aligned with geographic expansion within southern Africa in most tribes, followed by range expansion to tropical Africa and multiple dispersals out of Africa. Our robust phylogeny provides a framework for future studies aimed at understanding the role of macroevolutionary patterns and processes that generated Scrophulariaceae diversity.

Patterns and processes in the history of body size in turritelline gastropods, Jurassic to Recent

AbstractBody size is an important trait with implications for energy use and ecology as well as generation time and evolutionary rates. Turritelline gastropods are widely distributed through geologic time and space, making them an excellent group for evaluating macroevolutionary patterns. To evaluate the pattern of body-size change in turritelline gastropods, we compiled a dataset of shell lengths of 316 species of turritelline gastropods spanning the Jurassic to Recent. Type specimens were almost always significantly larger than specimen distributions from the same species. We found that turritelline gastropod size was inversely correlated with latitude, a trend likely driven by the Neogene–Recent diversification of small-bodied Southern Hemisphere taxa. A time series model was applied to distinguish among three possible macroevolutionary patterns: unbiased random walk (no directional trend), biased random walk (directional trend), and stasis (no net change). We determined that turritelline gastropods have experienced stasis in body size throughout their evolutionary history, adding to the growing literature documenting directionless body-size trends in marine invertebrate clades. Stasis of geographically widespread clades may be the result of ecological variability across the environmental range occupied by the group or differential diversification into opposing environments. Turritelline life-history patterns, especially their reproductive strategy that combines a short life span and decline in growth rate around 1 year of age to reallocate energy to reproduction, might circumvent selection for longevity and larger size, while further decrease in minimum size is likely limited by feeding efficiency and anti-predatory defense. The expectation that species or clades should continue to evolve to occupy larger size classes conflicts with the evolutionary advantages of small size, which in turritelline gastropods include high generational turnover and larger population sizes that yield opportunities for genetic variance.

Climate drives global functional trait variation in lizards.

A major challenge in ecology and evolution is to disentangle the mechanisms driving broad-scale variation in biological traits such as body size, colour, thermal physiology traits and behaviour. Climate has long been thought to drive trait evolution and abiotic filtering of trait variation in ectotherms because their thermal performance and fitness are closely related to environmental conditions. However, previous studies investigating climatic variables associated with trait variation have lacked a mechanistic description of the underpinning processes. Here, we use a mechanistic model to predict how climate affects thermal performance of ectotherms and thereby the direction and strength of the effect of selection on different functional traits. We show that climate drives macro-evolutionary patterns in body size, cold tolerance and preferred body temperatures among lizards, and that trait variation is more constrained in regions where selection is predicted to be stronger. These findings provide a mechanistic explanation for observations on how climate drives trait variation in ectotherms through its effect on thermal performance. By connecting physical, physiological and macro-evolutionary principles, the model and results provide an integrative, mechanistic framework for predicting organismal responses to present climates and climate change.

Diversification of the ruminant skull along an evolutionary line of least resistance.

Clarifying how microevolutionary processes scale to macroevolutionary patterns is a fundamental goal in evolutionary biology, but these analyses, requiring comparative datasets of population-level variation, are limited. By analyzing a previously published dataset of 2859 ruminant crania, we find that variation within and between ruminant species is biased by a highly conserved mammalian-wide allometric pattern, CREA (craniofacial evolutionary allometry), where larger species have proportionally longer faces. Species with higher morphological integration and species more biased toward CREA have diverged farther from their ancestors, and Ruminantia as a clade diversified farther than expected in the direction of CREA. Our analyses indicate that CREA acts as an evolutionary "line of least resistance" and facilitates morphological diversification due to its alignment with the browser-grazer continuum. Together, our results demonstrate that constraints at the population level can produce highly directional patterns of phenotypic evolution at the macroevolutionary scale. Further research is needed to explore how CREA has been exploited in other mammalian clades.

Estimating spatial variation in origination and extinction in deep time: a case study using the Permian–Triassic marine invertebrate fossil record

AbstractUnderstanding spatial variation in origination and extinction can help to unravel the mechanisms underlying macroevolutionary patterns. Although methods have been developed for estimating global origination and extinction rates from the fossil record, no framework exists for applying these methods to restricted spatial regions. Here, we test the efficacy of three metrics for regional analysis, using simulated fossil occurrences. These metrics are then applied to the marine invertebrate record of the Permian and Triassic to examine variation in extinction and origination rates across latitudes. Extinction and origination rates were generally uniform across latitudes for these time intervals, including during the Capitanian and Permian–Triassic mass extinctions. The small magnitude of this variation, combined with the possibility of its attribution to sampling bias, cautions against linking any observed differences to contrasting evolutionary dynamics. Our results indicate that origination and extinction levels were more variable across clades than across latitudes.

Bedrock geological map predictions for Phanerozoic fossil occurrences

AbstractGeographically explicit, taxonomically resolved fossil occurrences are necessary for reconstructing macroevolutionary patterns and for testing a wide range of hypotheses in the Earth and life sciences. Heterogeneity in the spatial and temporal distribution of fossil occurrences in the Paleobiology Database (PBDB) is attributable to several different factors, including turnover among biological communities, socioeconomic disparities in the intensity of paleontological research, and geological controls on the distribution and fossil yield of sedimentary deposits. Here we use the intersection of global geological map data from Macrostrat and fossil collections in the PBDB to assess the extent to which the potentially fossil-bearing, surface-expressed sedimentary record has yielded fossil occurrences. We find a significant and moderately strong positive correlation between geological map area and the number of fossil occurrences. This correlation is consistent regardless of map unit age and binning protocol, except at period level; the Neogene and Quaternary have non-marine map units covering large areas and yielding fewer occurrences than expected. The sedimentary record of North America and Europe yields significantly more fossil occurrences per sedimentary area than similarly aged deposits in most of the rest of the world. However, geographic differences in area and age of sedimentary deposits lead to regionally different expectations for fossil occurrences. Using the sampling of surface-expressed sedimentary units in North America and Europe as a predictor for what might be recoverable from the surface-expressed sedimentary deposits of other regions, we find that the rest of the globe is approximately 45% as well sampled in the PBDB. Using age and area of bedrock and sampling in North America and Europe as a basis for prediction, we estimate that more than 639,000 occurrences from outside these regions would need to be added to the PBDB to achieve global geological parity in sampling. In general, new terrestrial fossil occurrences are expected to have the greatest impact on our understanding of macroevolutionary patterns.

Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity.

Vertebrate limb morphology often reflects the environment due to variation in locomotor requirements. However, proximal and distal limb segments may evolve differently from one another, reflecting an anatomical gradient of functional specialization that has been suggested to be impacted by the timing of development. Here, we explore whether the temporal sequence of bone condensation predicts variation in the capacity of evolution to generate morphological diversity in proximal and distal forelimb segments across more than 600 species of mammals. Distal elements not only exhibit greater shape diversity, but also show stronger within-element integration and, on average, faster evolutionary responses than intermediate and upper limb segments. Results are consistent with the hypothesis that late developing distal bones display greater morphological variation than more proximal limb elements. However, the higher integration observed within the autopod deviates from such developmental predictions, suggesting that functional specialization plays an important role in driving within-element covariation. Proximal and distal limb segments also show different macroevolutionary patterns, albeit not showing a perfect proximo-distal gradient. The high disparity of the mammalian autopod, reported here, is consistent with the higher potential of development to generate variation in more distal limb structures, as well as functional specialization of the distal elements.

Dental topographic proxies for ecological characteristics in carnivoran mammals.

Form-function relationships in mammalian feeding systems are active topics of research in evolutionary biology. This is due principally to their fundamental importance for understanding dietary adaptations in extinct taxa and macro-evolutionary patterns of morphological transformations through changing environments. We hypothesize that three-dimensional dental topographic metrics represent stronger predictors for dietary and other ecological variables than do linear measurements. To test this hypothesis, we measured three dental topographic metrics: Relief Index (RFI), Dirichlet Normal Energy (DNE), and Orientation Patch Count Rotated (OPCR) in 57 extant carnivoran species. Premolar and molar dental topographic indices were regressed against activity, diet breadth, habitat breadth, terrestriality, and trophic level variables within a phylogenetic framework. The results of this study showed significant correlations between RFI and the ecological variables diet breadth and trophic level. Weaker correlations are documented between OPCR and activity and between DNE and trophic level. Our results suggest that cusp height is strongly reflective of dietary ecology in carnivorans as a whole, and represents a proxy mainly for different degrees of hypercarnivory observed within this group of predatory mammals.

Two large squirrels (Rodentia, Mammalia) from the Junggar Basin of northwestern China demonstrate early radiation among squirrels and suggest forested paleoenvironment in the late Eocene of Central Asia

Fossil evidence is indispensable for studying the derivation, divergence, and dispersal of squirrels as they responded to global Cenozoic climatic and paleoenvironmental change. Among these fossil records, the earliest known definitive fossil squirrels in Eurasia occur after the Eocene/Oligocene Boundary and are slightly younger than the oldest records in North America. Here, we report the discovery of two new extinct large squirrel species from the late Eocene of the Junggar Basin in northwestern China. The dental morphologies of these new taxa represent tree and flying morphotypes, and their estimated body masses are approximately 1.2 kg and 2.6 kg, respectively. In addition, these extinct lineages push the age of the first appearance of Sciuridae in northern Asia into the late Eocene. Together with Douglassciurus and Oligospermophilus from North America, these two new squirrels from the Junggar Basin are the earliest records of sciurids, and analysis of their teeth clearly demonstrates that the three principle morphotypes of sciurids (flying, ground, and tree squirrels) had diverged from one another by the late Eocene. That proposed late Eocene divergence among the major groupings of sciurids is consistent with some molecular clock analyses and helps to document that macroevolutionary timing and pattern. Comparison with modern squirrel analogs for body masses over 1 kg points to these early Chinese species as having occupied forested habitats, and that hypothesis is congruent with published palynological studies. Furthermore, these two new squirrel taxa from Jeminay provide new data to evaluate the examination of the long-term aridification of Central Asia.

Dental ecomorphology and macroevolutionary patterns of North American Late Cretaceous metatherians

Dental ecomorphology and macroevolutionary patterns of North American Late Cretaceous metatherians