Extinct and extant termites reveal the fidelity of behavior fossilization in amber.

Fossils encompassing multiple individuals provide rare direct evidence of behavioral interactions among extinct organisms. However, the fossilization process can alter the spatial relationship between individuals and hinder behavioral reconstruction. Here, we report a Baltic amber inclusion preserving a female-male pair of the extinct termite species Electrotermes affinis. The head-to-abdomen contact in the fossilized pair resembles the tandem courtship behavior of extant termites, although their parallel body alignment differs from the linear alignment typical of tandem runs. To solve this inconsistency, we simulated the first stage of amber formation, the immobilization of captured organisms, by exposing living termite tandems to sticky surfaces. We found that the posture of the fossilized pair matches trapped tandems and differs from untrapped tandems. Thus, the fossilized pair likely is a tandem running pair, representing the direct evidence of the mating behavior of extinct termites. Furthermore, by comparing the postures of partners on a sticky surface and in the amber inclusion, we estimated that the male likely performed the leader role in the fossilized tandem. Our results demonstrate that past behavioral interactions can be reconstructed despite the spatial distortion of body poses during fossilization. Our taphonomic approach demonstrates how certain behaviors can be inferred from fossil occurrences.

Teeth, prenatal growth rates, and the evolution of human-like pregnancy in later Homo.

Evidence of how gestational parameters evolved is essential to understanding this fundamental stage of human life. Until now, these data seemed elusive given the skeletal bias of the fossil record. We demonstrate that dentition provides a window into the life of neonates. Teeth begin to form in utero and are intimately associated with gestational development. We measured the molar dentition for 608 catarrhine primates and collected data on prenatal growth rate (PGR) and endocranial volume (ECV) for 19 primate genera from the literature. We found that PGR and ECV are highly correlated (R2 = 0.93, P < 0.001). Additionally, we demonstrated that molar proportions are significantly correlated with PGR (P = 0.004) and log-transformed ECV (P = 0.001). From these correlations, we developed two methods for reconstructing PGR in the fossil record, one using ECV and one using molar proportions. Dental proportions reconstruct hominid ECV (R2 = 0.81, P < 0.001), a result that can be extrapolated to PGR. As teeth dominate fossil assemblages, our findings greatly expand our ability to investigate life history in the fossil record. Fossil ECVs and dental measurements from 13 hominid species both support significantly increasing PGR throughout the terminal Miocene and Plio-Pleistocene, reflecting known evolutionary changes. Together with pelvic and endocranial morphology, reconstructed PGRs indicate the need for increasing maternal energetics during pregnancy over the last 6 million years, reaching a human-like PGR (i.e., more similar to humans than to other extant apes) and ECV in later Homo less than 1 million years ago.

Ad fontes: divergence-time estimation and the age of angiosperms.

Accurate divergence times are essential for interpreting and understanding the context in which lineages have evolved. Over the past several decades, debates have surrounded the discrepancies between the inferred molecular ages of crown angiosperms, often estimated from the Late Jurassic into the Permian, and the fossil record, placing angiosperms in the Early Cretaceous. That crown angiosperms could have emerged as early as the Permian or even the Triassic would have major implications for the paleoecological context of the origin of one of the most consequential clades in the tree of life. Here, we argue, and demonstrate through simulations, that the older ages inferred from molecular data and relaxed-clock models are misled by lineage-specific rate heterogeneity resulting from life history changes that occurred several times throughout the evolution of vascular plants. To overcome persistent discrepancies in age estimates, more biologically informed and realistic models should be developed, and our results should be considered in the context of their biological implications before we accept inferences that are a major departure from our strongest evidence.

Functional traits of fossil plants.

A minuscule fraction of the Earth's paleobiological diversity is preserved in the geological record as fossils. What plant remnants have withstood taphonomic filtering, fragmentation, and alteration in their journey to become part of the fossil record provide unique information on how plants functioned in paleo-ecosystems through their traits. Plant traits are measurable morphological, anatomical, physiological, biochemical, or phenological characteristics that potentially affect their environment and fitness. Here, we review the rich literature of paleobotany, through the lens of contemporary trait-based ecology, to evaluate which well-established extant plant traits hold the greatest promise for application to fossils. In particular, we focus on fossil plant functional traits, those measurable properties of leaf, stem, reproductive, or whole plant fossils that offer insights into the functioning of the plant when alive. The limitations of a trait-based approach in paleobotany are considerable. However, in our critical assessment of over 30 extant traits we present an initial, semi-quantitative ranking of 26 paleo-functional traits based on taphonomic and methodological criteria on the potential of those traits to impact Earth system processes, and for that impact to be quantifiable. We demonstrate how valuable inferences on paleo-ecosystem processes (pollination biology, herbivory), past nutrient cycles, paleobiogeography, paleo-demography (life history), and Earth system history can be derived through the application of paleo-functional traits to fossil plants.

How Important Is Budding Speciation for Comparative Studies?

The acknowledgment of evolutionary dependence among species has fundamentally changed how we ask biological questions. Phylogenetic models became the standard approach for studies with 3 or more lineages, in particular those using extant species. Most phylogenetic comparative methods (PCMs) translate relatedness into covariance, meaning that evolutionary changes before lineages split should be interpreted together whereas after the split lineages are expected to change independently. This clever realization has shaped decades of research. Here, we discuss one element of the comparative method often ignored or assumed as unimportant: if nodes of a phylogeny represent the dissolution of the ancestral lineage into two new ones or if the ancestral lineage can survive speciation events (i.e., budding). Budding speciation is often reported in paleontological studies, due to the nature of the evidence for budding in the fossil record, but it is surprisingly absent in comparative methods. Here, we show that many PCMs assume that divergence happens as a symmetric split, even if these methods do not explicitly mention this assumption. We discuss the properties of trait evolution models for continuous and discrete traits and their adequacy under a scenario of budding speciation. We discuss the effects of budding speciation under a series of plausible evolutionary scenarios and show when and how these can influence our estimates. We also propose that long-lived lineages that have survived through a series of budding speciation events and given birth to multiple new lineages can produce evolutionary patterns that challenge our intuition about the most parsimonious history of trait changes in a clade. We hope our discussion can help bridge comparative approaches in paleontology and neontology as well as foster awareness about the assumptions we make when we use phylogenetic trees.

Revisiting the sedimentary record of the rise of diatoms.

Diatoms are a major primary producer in the modern oceans and play a critical role in the marine silica cycle. Their rise to dominance is recognized as one of the largest shifts in Cenozoic marine ecosystems, but the timing of this transition is debated. Here, we use a diagenetic model to examine the effect of sedimentation rate and temperature on the burial efficiency of biogenic silica over the past 66 million years (i.e., the Cenozoic). We find that the changing preservation potential of siliceous microfossils during that time would have overprinted the primary signal of diatom and radiolarian abundance. We generate a taphonomic null hypothesis of the diatom fossil record by assuming a constant flux of diatoms to the sea floor and having diagenetic conditions driven by observed shifts in temperature and sedimentation rate. This null hypothesis produces a late Cenozoic (∼5 Ma to 20 Ma) increase in the relative abundance of fossilized diatoms that is comparable to current empirical records. This suggests that the observed increase in diatom abundance in the sedimentary record may be driven by changing preservation potential. A late Cenozoic rise in diatoms has been causally tied to the rise of grasslands and baleen whales and to declining atmospheric CO2 levels. Here we suggest that the similarity among these records primarily arises from a common driver-the cooling climate system-that drove enhanced diatom preservation as well as the rise of grasslands and whales, rather than a causal link among them.

Deep-time climate legacies affect origination rates of marine genera.

Biodiversity dynamics are shaped by a complex interplay between current conditions and historic legacy. The interaction of short- and long-term climate change may mask the true relationship of evolutionary responses to climate change if not specifically accounted for. These paleoclimate interactions have been demonstrated for extinction risk and biodiversity change, but their importance for origination dynamics remains untested. Here, we show that origination probability in marine fossil genera is strongly affected by paleoclimate interactions. Overall, origination probability increases by 27.8% [95% CI (27.4%, 28.3%)] when a short-term cooling adds to a long-term cooling trend. This large effect is consistent through time and all studied groups. The mechanisms of the detected effect might be manifold but are likely connected to increased allopatric speciation with eustatic sea level drop caused by sustained global cooling. We tested this potential mechanism through which paleoclimate interactions can act on origination rates by additionally examining a proxy for habitat fragmentation. This proxy, continental fragmentation, has a similar effect on origination rates as paleoclimate interactions, supporting the importance of allopatric speciation through habitat fragmentation in the deep-time fossil record. The identified complex nature of paleoclimate interactions might explain contradictory conclusions on the relationship between temperature and origination in the previous literature. Our results highlight the need to account for complex interactions in evolutionary studies both between and among biotic and abiotic factors.

What we talk about when we talk about the long-term carbon cycle.

The terrestrial biota is a crucial part of the long-term carbon cycle via the deposition of biomass as coal and other sedimentary organic matter and the impact of plants, fungi, and microbial life on the weathering of silicate minerals. Understanding these processes and their changes through time requires both geochemical modeling of the system as well as expertise in the living and fossil biotas and their ecological interactions, but details of these components are often lost in translation between disciplines. Here, we highlight misconceptions of the long-term carbon cycle that most frequently infiltrate the literature and hamper progress: mass balance requirements, the nature and duration of perturbations, opposing timescale constraints on biological and geological processes, and the role of models.

The origin and diversification of pteropods precede past perturbations in the Earth's carbon cycle.

Pteropods are a group of planktonic gastropods that are widely regarded as biological indicators for assessing the impacts of ocean acidification. Their aragonitic shells are highly sensitive to acute changes in ocean chemistry. However, to gain insight into their potential to adapt to current climate change, we need to accurately reconstruct their evolutionary history and assess their responses to past changes in the Earth's carbon cycle. Here, we resolve the phylogeny and timing of pteropod evolution with a phylogenomic dataset (2,654 genes) incorporating new data for 21 pteropod species and revised fossil evidence. In agreement with traditional taxonomy, we recovered molecular support for a division between "sea butterflies" (Thecosomata; mucus-web feeders) and "sea angels" (Gymnosomata; active predators). Molecular dating demonstrated that these two lineages diverged in the early Cretaceous, and that all main pteropod clades, including shelled, partially-shelled, and unshelled groups, diverged in the mid- to late Cretaceous. Hence, these clades originated prior to and subsequently survived major global change events, including the Paleocene-Eocene Thermal Maximum (PETM), the closest analog to modern-day ocean acidification and warming. Our findings indicate that planktonic aragonitic calcifiers have shown resilience to perturbations in the Earth's carbon cycle over evolutionary timescales.

Prominent Roles and Conflicted Attitudes of Eumelanin in the Living World.

Eumelanin, a macromolecule widespread in all the living world and long appreciated for its protective action against harmful UV radiation, is considered the beneficial component of the melanin family (ευ means good in ancient Greek). This initially limited picture has been rather recently extended and now includes a variety of key functions performed by eumelanin in order to support life also under extreme conditions. A lot of still unexplained aspects characterize this molecule that, in an evolutionary context, survived natural selection. This paper aims to emphasize the unique characteristics and the consequent unusual behaviors of a molecule that still holds the main chemical/physical features detected in fossils dating to the late Carboniferous. In this context, attention is drawn to the duality of roles played by eumelanin, which occasionally reverses its functional processes, switching from an anti-oxidant to a pro-oxidant behavior and implementing therefore harmful effects.

Sampling biases obscure the early diversification of the largest living vertebrate group.

Extant ray-finned fishes (Actinopterygii) dominate marine and freshwater environments, yet spatio-temporal diversity dynamics following their origin in the Palaeozoic are poorly understood. Previous studies investigate face-value patterns of richness, with only qualitative assessment of biases acting on the Palaeozoic actinopterygian fossil record. Here, we investigate palaeogeographic trends, reconstruct local richness and apply richness estimation techniques to a recently assembled occurrence database for Palaeozoic ray-finned fishes. We identify substantial fossil record biases, such as geographical bias in sampling centred around Europe and North America. Similarly, estimates of diversity are skewed by extreme unevenness in the occurrence distributions, reflecting historical biases in sampling and taxonomic practices, to the extent that evenness has an overriding effect on diversity estimates. Other than a genuine rise in diversity in the Tournaisian following the end-Devonian mass extinction, diversity estimates for Palaeozoic actinopterygians appear to lack biological signal, are heavily biased and are highly dependent on sampling. Increased sampling of poorly represented regions and expanding sampling beyond the literature to include museum collection data will be critical in obtaining accurate estimates of Palaeozoic actinopterygian diversity. In conjunction, applying diversity estimation techniques to well-sampled regional subsets of the 'global' dataset may identify accurate local diversity trends.

Do species factories exist? Detecting exceptional patterns of evolution in the mammalian fossil record.

A species factory refers to the source that gives rise to an exceptionally large number of species. However, what is it exactly: a place, a time or a combination of places, times and environmental conditions, remains unclear. Here we search for species factories computationally, for which we develop statistical approaches to detect origination, extinction and sorting hotspots in space and time in the fossil record. Using data on European Late Cenozoic mammals, we analyse where, how and how often species factories occur, and how they potentially relate to the dynamics of environmental conditions. We find that in the Early Miocene origination hotspots tend to be located in areas with relatively low estimated net primary productivity. Our pilot study shows that species first occurring in origination hotspots tend to have a longer average longevity and a larger geographical range than other species, thus emphasizing the evolutionary importance of the species factories.

The role of paleontological data in bryophyte systematics.

Systematics reconstructs tempo and mode in biological evolution by resolving the phylogenetic fabric of biodiversity. The staggering duration and complexity of evolution, coupled with loss of information (extinction), render exhaustive reconstruction of the evolutionary history of life unattainable. Instead, we sample its products-phenotypes and genotypes-to generate phylogenetic hypotheses, which we sequentially reassess and update against new data. Current consensus in evolutionary biology emphasizes fossil integration in total-evidence analyses, requiring in-depth understanding of fossils-age, phenotypes, and systematic affinities-and a detailed morphological framework uniting fossil and extant taxa. Bryophytes present a special case: deep evolutionary history but sparse fossil record and phenotypic diversity encompassing small dimensional scales. We review how these peculiarities shape fossil inclusion in bryophyte systematics. Paucity of the bryophyte fossil record, driven primarily by phenotypic (small plant size) and ecological constraints (patchy substrate-hugging populations), and incomplete exploration, results in many morphologically isolated, taxonomically ambiguous fossil taxa. Nevertheless, instances of exquisite preservation and pioneering studies demonstrate the feasibility of including bryophyte fossils in evolutionary inference. Further progress will arise from developing extensive morphological matrices for bryophytes, continued exploration of the fossil record, re-evaluation of previously described fossils, and training specialists in identification and characterization of bryophyte fossils, and in bryophyte morphology.

What is the age of flowering plants?

The origin of flowering plants (angiosperms) was one of the most transformative events in the history of our planet. Despite considerable interest from multiple research fields, numerous questions remain, including the age of the group as a whole. Recent studies have reported a perplexing range of estimates for the crown-group age of angiosperms, from ~140 million years (Ma; Early Cretaceous) to 270 Ma (Permian). Both ends of the spectrum are now supported by both macroevolutionary analyses of the fossil record and fossil-calibrated molecular dating analyses. Here, we first clarify and distinguish among the three ages of angiosperms: the age of their divergence with acrogymnosperms (stem age); the age(s) of emergence of their unique, distinctive features including flowers (morphological age); and the age of the most recent common ancestor of all their living species (crown age). We then demonstrate, based on recent studies, that fossil-calibrated molecular dating estimates of the crown-group age of angiosperms have little to do with either the amount of molecular data or the number of internal fossil calibrations included. Instead, we argue that this age is almost entirely conditioned by its own prior distribution (typically a calibration density set by the user in Bayesian analyses). Lastly, we discuss which future discoveries or novel types of analyses are most likely to bring more definitive answers. In the meantime, we propose that the age of angiosperms is best described as largely unknown (140-270 Ma) and that contrasting age estimates in the literature mostly reflect conflicting prior distributions. We also suggest that future work that depends on the time scale of flowering plant diversification be designed to integrate over this vexing uncertainty.

Rocks and clocks revised: New promises and challenges in dating the primate tree of life.

In recent years, multiple technological and methodological advances have increased our ability to estimate phylogenies, leading to more accurate dating of the primate tree of life. Here we provide an overview of the limitations and potentials of some of these advancements and discuss how dated phylogenies provide the crucial temporal scale required to understand primate evolution. First, we review new methods, such as the total-evidence dating approach, that promise a better integration between the fossil record and molecular data. We then explore how the ever-increasing availability of genomic-level data for more primate species can impact our ability to accurately estimate timetrees. Finally, we discuss more recent applications of mutation rates to date divergence times. We highlight example studies that have applied these approaches to estimate divergence dates within primates. Our goal is to provide a critical overview of these new developments and explore the promises and challenges of their application in evolutionary anthropology.

Reconstruction of the evolutionary biogeography reveal the origins and diversification of oysters (Bivalvia: Ostreidae).

Oysters (Bivalvia: Ostreidae Rafinesque, 1815) live in the intertidal and shallow subtidal areas worldwide. Despite their long evolutionary histories, abundant fossil records, global distribution, and ecological significance, a systematic time-dependent biogeographical analysis of this family is still lacking. Using combined mitochondrial (COI and 16S rRNA) and nuclear (18S rRNA, 28S rRNA, H3 and ITS2) gene makers for 80% (70/88) of the recognized extant Ostreidae, we reconstructed the global phylogenetic and biogeographical relationships throughout the evolutionary history of oysters. The result provided a holistic view of the origin, migration and dispersal patterns of Ostreidae. The phylogenetic results and fossil evidence indicated that Ostreidae originated from the circum-Arctic region in the Early Jurassic. The widening of the Atlantic Ocean and changes in the Tethys Ocean further facilitated their subsequent diversification during the Cretaceous and the Palaeogene periods. In particular, Crassostrea and Saccostrea exhibited relatively low dispersal abilities and their major diversifications were consistent with the tectonic events. Environmental adaptations and reproductive patterns, therefore, should play key roles in the formation of oyster distribution patterners, rather than the dispersal ability of their planktonic larvae. The diversity dynamics inferred by standard phylogenetic are consistent with the fossil record, however, further systematic classification, especially for fossil genus Ostrea, would enhance our understanding on extant and fossil oysters. The present study of the historical biogeography of oysters provides new insights into the evolution and speciation of oysters. Our findings also provide a foundation for the assessment of evolutionary patterns and ecological processes in intertidal and inshore life.

First Bignoniaceae liana from the Miocene of South America and its evolutionary significance.

PREMISE: Two Bignoniaceae stems with the distinctive anatomy of a liana are described from the Miocene of South America. They are the first fossil evidence of climbing habit in Bignoniaceae. METHODS: The fossil lianas are siliceous permineralizations. Transverse, tangential, and radial thin sections of the woods were prepared for study using standard petrographic techniques and observed under both light and scanning electron microscopy. RESULTS: The stems consist of wood and presumably bark (peripheral tissues). They exhibit phloem wedges, a cambial variant associated with the climbing habit in Bignoniaceae. The wood is diffuse-porous; solitary and in radial multiples vessels; alternated intervessel pitting; ray-vessel pitting with distinct borders; simple perforation plates; rays 1-3 seriate, composed of procumbent cells or body ray cells procumbent with one or two-row of upright or square marginal cells; fibers septate and non-septate, with simple to minutely bordered pits; axial parenchyma scanty paratracheal, vasicentric, septate; perforated ray cells; prismatic crystals in rays, and rays and fibers irregularly storied. The fossil stems are related to extant Dolichandra unguis-cati (L.) Miers. CONCLUSIONS: The fossils represent a new taxon, Dolichandra pacei sp. nov., which confirms the presence of a neotropical Bignoniaceae liana from the Miocene and provides the first and oldest evidence of the climbing habit in the family. Paleobotanical studies in the Mariño Formation, with the record of Bignoniaceae and Verbenaceae, and phylogenetic and biogeographical studies have great importance to understand plant evolution and diversification in South American Andes.

The origin of Darwin's "abominable mystery".

The phrase "Darwin's abominable mystery" is frequently used with reference to a range of outstanding questions about the evolution of the plant group today known as the angiosperms. Here, I seek to more fully understand what prompted Darwin to coin the phrase in 1879, and the meaning he attached to it, by surveying the systematics, paleobotanical records, and phylogenetic hypotheses of his time. In the light of this historical research, I argue that Darwin was referring to the origin only of a subset of what are today called angiosperms: a (now obsolete) group equivalent to the "dicotyledons" of the Hooker and Bentham system. To Darwin and his contemporaries, the dicotyledons' fossil record began abruptly and with great diversity in the Cretaceous, whereas the gymnosperms and monocotyledons were thought to have fossil records dating back to the Carboniferous or beyond. Based on their morphology, the dicotyledons were widely seen by botanists in Darwin's time (unlike today) as more similar to the gymnosperms than to the monocotyledons. Thus, morphology seemed to point to gymnosperm progenitors of dicotyledons, but this hypothesis made the monocotyledons, given their (at the time) apparently longer fossil record, difficult to place. Darwin had friendly disagreements about the mystery of the dicotyledons' abrupt appearance in the fossil record with others who thought that their evolution must have been more rapid than his own gradualism would allow. But the mystery may have been made "abominable" to him because it was seen by some contemporary paleobotanists, most notably William Carruthers, the Keeper of Botany at the British Museum, as evidence for divine intervention in the history of life. Subsequent developments in plant systematics and paleobotany after 1879 meant that Darwin's letter was widely understood to be referring to the abrupt appearance of all angiosperms when it was published in 1903, a meaning that has been attached to it ever since.

Arthropods in modern resins reveal if amber accurately recorded forest arthropod communities.

Amber is an organic multicompound derivative from the polymerization of resin of diverse higher plants. Compared with other modes of fossil preservation, amber records the anatomy of and ecological interactions between ancient soft-bodied organisms with exceptional fidelity. However, it is currently suggested that ambers do not accurately record the composition of arthropod forest paleocommunities, due to crucial taphonomic biases. We evaluated the effects of taphonomic processes on arthropod entrapment by resin from the plant Hymenaea, one of the most important resin-producing trees and a producer of tropical Cenozoic ambers and Anthropocene (or subfossil) resins. We statistically compared natural entrapment by Hymenaea verrucosa tree resin with the ensemble of arthropods trapped by standardized entomological traps around the same tree species. Our results demonstrate that assemblages in resin are more similar to those from sticky traps than from malaise traps, providing an accurate representation of the arthropod fauna living in or near the resiniferous tree, but not of entire arthropod forest communities. Particularly, arthropod groups such as Lepidoptera, Collembola, and some Diptera are underrepresented in resins. However, resin assemblages differed slightly from sticky traps, perhaps because chemical compounds in the resins attract or repel specific insect groups. Ground-dwelling or flying arthropods that use the tree-trunk habitat for feeding or reproduction are also well represented in the resin assemblages, implying that fossil inclusions in amber can reveal fundamental information about biology of the past. These biases have implications for the paleoecological interpretation of the fossil record, principally of Cenozoic amber with angiosperm origin.

Sporadic sampling, not climatic forcing, drives observed early hominin diversity.

The role of climate change in the origin and diversification of early hominins is hotly debated. Most accounts of early hominin evolution link observed fluctuations in species diversity to directional shifts in climate or periods of intense climatic instability. None of these hypotheses, however, have tested whether observed diversity patterns are distorted by variation in the quality of the hominin fossil record. Here, we present a detailed examination of early hominin diversity dynamics, including both taxic and phylogenetically corrected diversity estimates. Unlike past studies, we compare these estimates to sampling metrics for rock availability (hominin-, primate-, and mammal-bearing formations) and collection effort, to assess the geological and anthropogenic controls on the sampling of the early hominin fossil record. Taxic diversity, primate-bearing formations, and collection effort show strong positive correlations, demonstrating that observed patterns of early hominin taxic diversity can be explained by temporal heterogeneity in fossil sampling rather than genuine evolutionary processes. Peak taxic diversity at 1.9 million years ago (Ma) is a sampling artifact, reflecting merely maximal rock availability and collection effort. In contrast, phylogenetic diversity estimates imply peak diversity at 2.4 Ma and show little relation to sampling metrics. We find that apparent relationships between early hominin diversity and indicators of climatic instability are, in fact, driven largely by variation in suitable rock exposure and collection effort. Our results suggest that significant improvements in the quality of the fossil record are required before the role of climate in hominin evolution can be reliably determined.