Deep Timescales Research Articles

Phylogenomic conflict coincides with rapid morphological innovation

Evolutionary biologists have long been fascinated with the episodes of rapid phenotypic innovation that underlie the emergence of major lineages. Although our understanding of the environmental and ecological contexts of such episodes has steadily increased, it has remained unclear how population processes contribute to emergent macroevolutionary patterns. One insight gleaned from phylogenomics is that gene-tree conflict, frequently caused by population-level processes, is often rampant during the origin of major lineages. With the understanding that phylogenomic conflict is often driven by complex population processes, we hypothesized that there may be a direct correspondence between instances of high conflict and elevated rates of phenotypic innovation if both patterns result from the same processes. We evaluated this hypothesis in six clades spanning vertebrates and plants. We found that the most conflict-rich regions of these six clades also tended to experience the highest rates of phenotypic innovation, suggesting that population processes shaping both phenotypic and genomic evolution may leave signatures at deep timescales. Closer examination of the biological significance of phylogenomic conflict may yield improved connections between micro- and macroevolution and increase our understanding of the processes that shape the origin of major lineages across the Tree of Life.

Anthropogenic heathlands: disturbance ecologies and the social organisation of past super-resilient landscapes

Focusing on the North European heathlands, this project investigates how self-organised communities in the past established large-scale grazing regimes. By considering changes in their particular forms of disturbance, exhaustion, autonomy and collaboration, the author envisages a new archaeology of emergent multispecies entanglements across a deep-time scale.

The emergence and intensification of early hunter-gatherer niche construction.

Hunter-gatherers, especially Pleistocene examples, are not well-represented in archeological studies of niche construction. However, as the role of humans in shaping environments over long time scales becomes increasingly apparent, it is critical to develop archeological proxies and testable hypotheses about early hunter-gatherer impacts. Modern foragers engage in niche constructive behaviors aimed at maintaining or increasing the productivity of their environments, and these may have had significant ecological consequences over later human evolution. In some cases, they may also represent behaviors unique to modern Homo sapiens. Archeological and paleoenvironmental data show that African hunter-gatherers were niche constructors in diverse environments, which have legacies in how ecosystems function today. These can be conceptualized as behaviorally mediated trophic cascades, and tested using archeological and paleoenvironmental proxies. Thus, large-scale niche construction behavior is possible to identify at deeper time scales, and may be key to understanding the emergence of modern humans.

Ecological Interactions and Macroevolution: A New Field with Old Roots

Linking interspecific interactions (e.g., mutualism, competition, predation, parasitism) to macroevolution (evolutionary change on deep timescales) is a key goal in biology. The role of species interactions in shaping macroevolutionary trajectories has been studied for centuries and remains a cutting-edge topic of current research. However, despite its deep historical roots, classic and current approaches to this topic are highly diverse. Here, we combine historical and contemporary perspectives on the study of ecological interactions in macroevolution, synthesizing ideas across eras to build a zoomed-out picture of the big questions at the nexus of ecology and macroevolution. We discuss the trajectory of this important and challenging field, dividing research into work done before the 1970s, research between 1970 and 2005, and work done since 2005. We argue that in response to long-standing questions in paleobiology, evidence accumulated to date has demonstrated that biotic interactions (including mutualism) can influence lineage diversification and trait evolution over macroevolutionary timescales, and we outline major open questions for future research in the field.

Songs versus colours versus horns: what explains the diversity of sexually selected traits?

Papers on sexual selection often highlight the incredible diversity of sexually selected traits across animals. Yet, few studies have tried to explain why this diversity evolved. Animals use many different types of traits to attract mates and outcompete rivals, including colours, songs, and horns, but it remains unclear why, for example, some taxa have songs, others have colours, and others horns. Here, we first conduct a systematic survey of the basic diversity and distribution of different types of sexually selected signals and weapons across the animal Tree of Life. Based on this survey, we describe seven major patterns in trait diversity and distributions. We then discuss 10 unanswered questions raised by these patterns, and how they might be addressed. One major pattern is that most types of sexually selected signals and weapons are apparently absent from most animal phyla (88%), in contrast to the conventional wisdom that a diversity of sexually selected traits is present across animals. Furthermore, most trait diversity is clustered in Arthropoda and Chordata, but only within certain clades. Within these clades, many different types of traits have evolved, and many types appear to have evolved repeatedly. By contrast, other major arthropod and chordate clades appear to lack all or most trait types, and similar patterns are repeated at smaller phylogenetic scales (e.g. within insects). Although most research on sexual selection focuses on female choice, we find similar numbers of traits (among sampled species) are involved in male contests (44%) and female choice (55%). Overall, these patterns are largely unexplained and unexplored, as are many other fundamental questions about the evolution of these traits. We suggest that understanding the diversity of sexually selected traits may require a shift towards macroevolutionary studies at relatively deep timescales (e.g. tens to hundreds of millions of years ago).

The origins of acoustic communication in vertebrates

Acoustic communication is crucial to humans and many other tetrapods, including birds, frogs, crocodilians, and mammals. However, large-scale patterns in its evolution are largely unstudied. Here, we address several fundamental questions about the origins of acoustic communication in terrestrial vertebrates (tetrapods), using phylogenetic methods. We show that origins of acoustic communication are significantly associated with nocturnal activity. We find that acoustic communication does not increase diversification rates, a surprising result given the many speciation-focused studies of frog calls and bird songs. We also demonstrate that the presence of acoustic communication is strongly conserved over time. Finally, we find that acoustic communication evolved independently in most major tetrapod groups, often with remarkably ancient origins (~100–200 million years ago). Overall, we show that the role of ecology in shaping signal evolution applies to surprisingly deep timescales, whereas the role of signal evolution in diversification may not.

Understanding UCEs: A Comprehensive Primer on Using Ultraconserved Elements for Arthropod Phylogenomics

Abstract Targeted enrichment of ultraconserved elements (UCEs) has emerged as a promising tool for inferring evolutionary history in many taxa, with utility ranging from phylogenetic and biogeographic questions at deep time scales to population level studies at shallow time scales. However, the methodology can be daunting for beginners. Our goal is to introduce UCE phylogenomics to a wider audience by summarizing recent advances in arthropod research, and to familiarize readers with background theory and steps involved. We define terminology used in association with the UCE approach, evaluate current laboratory and bioinformatic methods and limitations, and, finally, provide a roadmap of steps in the UCE pipeline to assist phylogeneticists in making informed decisions as they employ this powerful tool. By facilitating increased adoption of UCEs in phylogenomics studies that deepen our comprehension of the function of these markers across widely divergent taxa, we aim to ultimately improve understanding of the arthropod tree of life.

Evolution of diet across the animal tree of life.

What an animal eats is a fundamental aspect of its biology, but the evolution of diet has not been studied across animal phylogeny. Here, we performed a large‐scale phylogenetic analysis to address three unresolved questions about the evolution of animal diets. (i) Are diets conserved across animal phylogeny? (ii) Does diet influence rates of species proliferation (diversification) among animal phyla? (iii) What was the ancestral diet of animals and major animal clades? We analyzed diet data for 1087 taxa, proportionally sampled among animal phyla based on the relative species richness of phyla. Our survey suggests that across animals, carnivory is most common (∼63%), herbivory less common (∼32%), and omnivory relatively rare (∼3%). Despite considerable controversy over whether ecological traits are conserved or labile, we found strong conservatism in diet over extraordinarily deep timescales. We found that diet is unrelated to rates of species diversification across animal phyla, contrasting with previous studies showing that herbivory increased diversification within some important groups (e.g., crustaceans, insects, and mammals). Finally, we estimated that the ancestor of all animals was most likely carnivorous, as were many major phyla (e.g., arthropods, molluscs, and chordates). Remarkably, our results suggest that many carnivorous species living today may have maintained this diet through a continuous series of carnivorous ancestors for >800 million years.

Evolution of DNA Methylation in Papio Baboons.

Changes in gene regulation have long been thought to play an important role in primate evolution. However, although a number of studies have compared genome-wide gene expression patterns across primate species, fewer have investigated the gene regulatory mechanisms that underlie such patterns, or the relative contribution of drift versus selection. Here, we profiled genome-scale DNA methylation levels in blood samples from five of the six extant species of the baboon genus Papio (4-14 individuals per species). This radiation presents the opportunity to investigate DNA methylation divergence at both shallow and deeper timescales (0.380-1.4 My). In contrast to studies in human populations, but similar to studies in great apes, DNA methylation profiles clearly mirror genetic and geographic structure. Divergence in DNA methylation proceeds fastest in unannotated regions of the genome and slowest in regions of the genome that are likely more constrained at the sequence level (e.g., gene exons). Both heuristic approaches and Ornstein-Uhlenbeck models suggest that DNA methylation levels at a small set of sites have been affected by positive selection, and that this class is enriched in functionally relevant contexts, including promoters, enhancers, and CpG islands. Our results thus indicate that the rate and distribution of DNA methylation changes across the genome largely mirror genetic structure. However, at some CpG sites, DNA methylation levels themselves may have been a target of positive selection, pointing to loci that could be important in connecting sequence variation to fitness-related traits.

Miocene biome turnover drove conservative body size evolution across Australian vertebrates.

On deep time scales, changing climatic trends can have a predictable influence on macroevolution. From evidence of mass extinctions, we know that rapid climatic oscillations can indirectly open niche space and precipitate adaptive radiation, changing the course of ecological diversification. These dramatic shifts in the global climate, however, are rare events relative to extended periods of protracted climate change and biome turnover. It remains unclear whether during gradually changing periods, shifting habitats may instead promote non-adaptive speciation by facilitating allopatry and phenotypic conservatism. Using fossil-calibrated, species-level phylogenies for five Australian radiations comprising more than 800 species, we investigated temporal trends in biogeography and body size evolution. Here, we demonstrate that gradual Miocene cooling and aridification correlates with the restricted phenotypic diversification of multiple ecologically diverse vertebrate groups. This probably occurred as species ranges became fractured and isolated during continental biome restructuring, encouraging a shift towards conservatism in body size evolution. Our results provide further evidence that abiotic changes, not only biotic interactions, may act as selective forces influencing phenotypic macroevolution.

High-throughput inference of pairwise coalescence times identifies signals of selection and enriched disease heritability.

Interest in reconstructing demographic histories has motivated the development of methods to estimate locus-specific pairwise coalescence times from whole-genome sequence data. Here we introduce a powerful new method, ASMC, that can estimate coalescence times using only SNP array data, and is orders of magnitude faster than previous approaches. We applied ASMC to detect recent positive selection in 113,851 phased British samples from the UK Biobank, and detected 12 genome-wide significant signals, including 6 novel loci. We also applied ASMC to sequencing data from 498 Dutch individuals to detect background selection at deeper time scales. We detected strong heritability enrichment in regions of high background selection in an analysis of 20 independent diseases and complex traits using stratified LD score regression, conditioned on a broad set of functional annotations (including other background selection annotations). These results underscore the widespread effects of background selection on the genetic architecture of complex traits.

Exon-Capture-Based Phylogeny and Diversification of the Venomous Gastropods (Neogastropoda, Conoidea).

Transcriptome-based exon capture methods provide an approach to recover several hundred markers from genomic DNA, allowing for robust phylogenetic estimation at deep timescales. We applied this method to a highly diverse group of venomous marine snails, Conoidea, for which published phylogenetic trees remain mostly unresolved for the deeper nodes. We targeted 850 protein coding genes (678,322 bp) in ca. 120 samples, spanning all (except one) known families of Conoidea and a broad selection of non-Conoidea neogastropods. The capture was successful for most samples, although capture efficiency decreased when DNA libraries were of insufficient quality and/or quantity (dried samples or low starting DNA concentration) and when targeting the most divergent lineages. An average of 75.4% of proteins was recovered, and the resulting tree, reconstructed using both supermatrix (IQ-tree) and supertree (Astral-II, combined with the Weighted Statistical Binning method) approaches, are almost fully supported. A reconstructed fossil-calibrated tree dates the origin of Conoidea to the Lower Cretaceous. We provide descriptions for two new families. The phylogeny revealed in this study provides a robust framework to reinterpret changes in Conoidea anatomy through time. Finally, we used the phylogeny to test the impact of the venom gland and radular type on diversification rates. Our analyses revealed that repeated losses of the venom gland had no effect on diversification rates, while families with a breadth of radula types showed increases in diversification rates, thus suggesting that trophic ecology may have an impact on the evolution of Conoidea.

Paleocene–Eocene and Plio–Pleistocene sea-level changes as “species pumps” in Southeast Asia: Evidence from Althepus spiders

Sea-level change has been viewed as a primary driver in the formation of biodiversity. Early studies confirmed that Plio–Pleistocene sea-level changes led to the isolation and subsequent genetic differentiation of Southeast (SE) Asian organisms over short geological timescales. However, long-time consequences of sea-level fluctuations remain unclear. Herein, we analyze the evolutionary history of Althepus (spiders) whose distribution encompasses Indo-Burma and the Sunda shelf islands to understand how sea-level changes over shallow and deep timescales effected their history. Our integrative analyses, including phylogeny, divergence times, ancestral area reconstruction and diversification dynamics, reveal an intricate pattern of diversification, probably triggered by sea-level fluctuations during the Paleocene–Eocene and Plio–Pleistocene. The timing of one early divergence between the Indo-Burmese and Sundaic species coincides with late Paleocene and early Eocene high global sea levels, which induced the formation of inland seaways in the Thai-Malay Peninsula. Subsequent lowered sea levels could have provided a land bridge for its dispersal colonization across the Isthmus of Kra. Analyses suggest that Plio–Pleistocene sea-level rises contributed to recent divergence of many species. Thus, our findings cannot reject the hypothesis that sea-level changes during the Paleocene–Eocene and Plio–Pleistocene played a major role in generating biodiversity in SE Asia; sea-level changes can act as “species pumps”.

Explaining Religion(s) with Deep Historical Time Scales

Explaining Religion(s) with Deep Historical Time Scales: A Comment from Cognitive Archaeology

Multilocus phylogenetic analysis of the first molecular data from the rare and monotypic Amarsipidae places the family within the Pelagia and highlights limitations of existing data sets in resolving pelagian interrelationships

The Pelagia is a recently delineated group of fishes, comprising fifteen families formerly placed in six perciform suborders. The Pelagia was lately recognized as it encompasses huge morphological diversity and only in the last few years have large-scale molecular phylogenetic studies been undertaken that could unite such morphologically disparate lineages. Due to the recent erection of Pelagia, the composition of the taxon is not entirely certain. Five families of the former perciform suborder Stromateoidei have been identified as pelagians. However, the sixth stromateoid subfamily Amarsipidae is a rare monotypic family that has distinctive meristic and morphological characteristics from that of other stromateoids such as the lack of a pharyngeal sac. We examine molecular data generated from the sole species in Amarsipidae, Amarsipus carlsbergi, and demonstrate that it is clearly nested within Pelagia. As with two previous studies that have the breadth of sampling to evaluate pelagian intra-relationships, we find high support for monophyly of most family-level taxonomic units but statistical support for early-branching nodes in the pelagian tree is very low. We conduct the first analyses of Pelagia incorporating the multispecies coalescent and are limited by a high degree of missing loci, or, incomplete taxon sampling. The high degree of missing data across a complete sampling of pelagian lineages along with the deep time scale and rapid radiation of the lineage contribute to poor resolution of early-branching relationships within Pelagia that cannot be resolved with current data sets. Currently available data are either mitochondrial genomes or a super matrix of relatively few loci with a high degree of missing data. A new and independent dataset of numerous phylogenetic loci derived from high-throughput sequencing technology may reduce uncertainty within the Pelagia and provide insights into this adaptive radiation.

Trait‐specific processes of convergence and conservatism shape ecomorphological evolution in ground‐dwelling squirrels

Our understanding of mechanisms operating over deep timescales to shape phenotypic diversity often hinges on linking variation in one or few trait(s) to specific evolutionary processes. When distinct processes are capable of similar phenotypic signatures, however, identifying these drivers is difficult. We explored ecomorphological evolution across a radiation of ground-dwelling squirrels whose history includes convergence and constraint, two processes that can yield similar signatures of standing phenotypic diversity. Using four ecologically relevant trait datasets (body size, cranial, mandibular, and molariform tooth shape), we compared and contrasted variation, covariation, and disparity patterns in a new phylogenetic framework. Strong correlations existed between body size and two skull traits (allometry) and among skull traits themselves (integration). Inferred evolutionary modes were also concordant across traits (Ornstein-Uhlenbeck with two adaptive regimes). However, despite these broad similarities, we found divergent dynamics on the macroevolutionary landscape, with phenotypic disparity being differentially shaped by convergence and conservatism. Such among-trait heterogeneity in process (but not always pattern) reiterates the mosaic nature of morphological evolution, and suggests ground squirrel evolution is poorly captured by single process descriptors. Our results also highlight how use of single traits can bias macroevolutionary inference, affirming the importance of broader trait-bases in understanding phenotypic evolutionary dynamics.

How sea level change mediates genetic divergence in coastal species across regions with varying tectonic and sediment processes.

Platetectonics and sediment processes control regional continental shelf topography. We examine the genetic consequences of how glacial-associated sea level change interacted with variable nearshore topography since the last glaciation. We reconstructed the size and distribution of areas suitable for tidal estuary formation from the last glacial maximum, ~20 thousand years ago, to present from San Francisco, California, USA (~38°N) to Reforma, Sinaloa, Mexico (~25°N). We assessed range-wide genetic structure and diversity of three codistributed tidal estuarine fishes (California Killifish, Shadow Goby, Longjaw Mudsucker) along ~4,600km using mitochondrial control region and cytB sequence, and 16-20 microsatellite loci from a total of 524 individuals. Results show that glacial-associated sea level change limited estuarine habitat to few, widely separated refugia at glacial lowstand, and present-day genetic clades were sourced from specific refugia. Habitat increased during postglacial sea level rise and refugial populations admixed in newly formed habitats. Continental shelves with active tectonics and/or low sediment supply were steep and hosted fewer, smaller refugia with more genetically differentiated populations than on broader shelves. Approximate Bayesian computation favoured the refuge-recolonization scenarios from habitat models over isolation by distance and seaway alternatives, indicating isolation at lowstand is a major diversification mechanism among these estuarine (and perhaps other) coastal species. Because sea level change is a global phenomenon, we suggest this top-down physical control of extirpation-isolation-recolonization may be an important driver of genetic diversification in coastal taxa inhabiting other topographically complex coasts globally during the Mid- to Late Pleistocene and deeper timescales.

Adapting to hurricanes. A historical perspective on New Orleans from its foundation to Hurricane Katrina, 1718–2005

Recent policy debates on climate change have started highlighting the importance of adaptation of societies to new conditions projected by climate scientists. Previously, mitigation had been almost the sole focus of policy‐makers for fear of creating a moral hazard when concentrating more strongly on adaptation. Yet, with many of the climatic changes the Intergovernmental Panel on Climate Change (IPCC) projected occurring faster than scientists predicted, adaptation has re‐entered the debate as an imperative. In this context, in which adaptation—a process often unfolding on deep timescales—becomes prescriptive, it is crucial to look at the historical development of adaptive practices over the long term in order to appreciate the complexity of their evolution. This paper is a hybrid between a summary of a research project and a review of the most crucial literature on which it was based. The point of departure of this study was Hurricane Katrina, which, after it had flooded New Orleans on August 29, 2005, raised the question, how such a disaster could have happened in one of the most technologically advanced nations in the world. I then rewind to the foundation of the city in 1718 and work my way along case studies through three centuries of hurricane history in New Orleans. The red thread is the concept of adaptation. I review the definition of adaptation provided by the Fifth Assessment Report of the IPCC from a historian's point of view and suggest a slight change of perspective. Knowledge as a precondition for adaptation, contingency, path‐dependence, political vulnerability, and the interplay of cultural, legal, and political factors emerge as crucial characteristics in the historical evolution of adaptive practices throughout the almost 300‐year period of study. WIREs Clim Change 2018, 9:e488. doi: 10.1002/wcc.488This article is categorized under: Climate, History, Society, Culture > World Historical Perspectives

Out of the dark: 350 million years of conservatism and evolution in diel activity patterns in vertebrates.

Many animals are active only during a particular time (e.g., day vs. night), a partitioning that may have important consequences for species coexistence. An open question is the extent to which this diel activity niche is evolutionarily conserved or labile. Here, we analyze diel activity data across a phylogeny of 1914 tetrapod species. We find strong phylogenetic signal, showing that closely related species tend to share similar activity patterns. Ancestral reconstructions show that nocturnality was the most likely ancestral diel activity pattern for tetrapods and many major clades within it (e.g., amphibians, mammals). Remarkably, nocturnal activity appears to have been maintained continuously in some lineages for ∼350 million years. Thus, we show that traits involved in local-scale resource partitioning can be conserved over strikingly deep evolutionary time scales. We also demonstrate a potentially important (but often overlooked) metric of niche conservatism. Finally, we show that diurnal lineages appear to have faster speciation and diversification rates than nocturnal lineages, which may explain why there are presently more diurnal tetrapod species even though diurnality appears to have evolved more recently. Overall, our results may have implications for studies of community ecology, species richness, and the evolution of diet and communication systems.

Global dynamics of dispersal and diversification among passerine birds

Explaining global variation in geographic and taxonomic diversity gradients represents a central focus of macroecology and macroevolution. Ultimately, these diversity gradients have been generated over deep timescales as a consequence of historical variation in rates of dispersal, diversification, and the capacity of different geographic areas to preserve taxa through time. Here, I assess the relationships among these processes, to elucidate the causes of geographic and taxonomic variation in species richness among the most speciose order of birds: the Passeriformes (c. 6,500 species). To achieve this, I comparatively analyze phylogenetic, distributional and eco-morphological trait data collated at broad taxonomic and spatial scales. The results of my analyses strongly support the prevalence of historical dispersal events across large geographic scales, in addition to spatiotemporal variation in diversification rates. These findings reflect that some lineages and some geographic regions (notably tropical mountain regions and island archipelagoes) generate and maintain a much larger amount of species diversity than others. In addition, the evolution of particular life-history and eco-morphological traits, specifically pair breeding systems, and higher wing aspect-ratios, increased rates of range expansion and diversification. In summary, geographic variation in historical diversification combined with differences in the capacity of lineages to colonize new areas, determines spatial and taxonomic differences in passerine species richness.