skip to main content


Title: A global phylogeny of turtles reveals a burst of climate-associated diversification on continental margins

Living turtles are characterized by extraordinarily low species diversity given their age. The clade’s extensive fossil record indicates that climate and biogeography may have played important roles in determining their diversity. We investigated this hypothesis by collecting a molecular dataset for 591 individual turtles that, together, represent 80% of all turtle species, including representatives of all families and 98% of genera, and used it to jointly estimate phylogeny and divergence times. We found that the turtle tree is characterized by relatively constant diversification (speciation minus extinction) punctuated by a single threefold increase. We also found that this shift is temporally and geographically associated with newly emerged continental margins that appeared during the Eocene−Oligocene transition about 30 million years before present. In apparent contrast, the fossil record from this time period contains evidence for a major, but regional, extinction event. These seemingly discordant findings appear to be driven by a common global process: global cooling and drying at the time of the Eocene−Oligocene transition. This climatic shift led to aridification that drove extinctions in important fossil-bearing areas, while simultaneously exposing new continental margin habitat that subsequently allowed for a burst of speciation associated with these newly exploitable ecological opportunities.

 
more » « less
Award ID(s):
1920304
NSF-PAR ID:
10213147
Author(s) / Creator(s):
; ;
Publisher / Repository:
Proceedings of the National Academy of Sciences
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Volume:
118
Issue:
7
ISSN:
0027-8424
Page Range / eLocation ID:
Article No. e2012215118
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Understanding the relationships between functional traits and environment is increasingly important for assessing ecosystem health and forecasting biotic responses to future environmental change. Taxon-free analyses of functional traits (ecometrics) allow for testing the performance of such traits through time, utilizing both the fossil record and paleoenvironmental proxies. Here, we test the role of body size as a functional trait with respect to climate, using turtles as a model system. We examine the influence of mass-specific metabolic rate as a functional factor in the sorting of body size with environmental temperature and investigate the utility of community body size composition as an ecometric correlated to climate variables. We then apply our results to the fossil record of the Plio-Pleistocene Shungura Formation in Ethiopia. Results show that turtle body sizes scale with mass-specific metabolic rate for larger taxa, but not for the majority of species, indicating that metabolism is not a primary driver of size. Body size ecometrics have stronger predictive power at continental than at global scales, but without a single, dominant predictive functional relationship. Application of ecometrics to the Shungura fossil record suggests that turtle paleocommunity ecometrics coarsely track independent paleoclimate estimates at local scales. We hypothesize that both human disruption and biotic interactions limit the ecometric fit of size to climate in this clade. Nonetheless, examination of the consistency of trait–environment relationships through deep and shallow time provides a means for testing anthropogenic influences on ecosystems.

     
    more » « less
  2. Abstract

    Saxochelys gilbertiis a baenid turtle from the Late Cretaceous Hell Creek Formation of the United States of America known from cranial, shell, and other postcranial material. Baenid turtles are taxonomically diverse and common fossil elements within Late Cretaceous through Eocene faunas. Detailed anatomical knowledge is critical to understanding the systematics and morphological evolution of the group. This is particularly important as baenids represent an important group of continental vertebrates that survived the mass extinction event associated with the Cretaceous/Paleogene boundary. High-resolution micro-computed tomography scanning of the holotype skull reveals additional anatomical details for the already well-knownSaxochelys gilberti. This includes the revision of some anatomical statements from the original description, but also detailed knowledge on internal anatomical features of the braincase and the description of a well-preserved axis (cervical vertebra 2). Our new detailed description and previous work on the shell and postcrania makeSaxochelysone of the best-described, nearly complete baenid turtles, which are often only known from either isolated shell or cranial material. A revised phylogenetic analysis confirms the position ofSaxochelys gilbertias a derived baenid (Eubaeninae) more closely related toBaena arenosathan toEubaena cephalica.

     
    more » « less
  3. Abstract

    Nyssa(Nyssaceae, Cornales) represents a classical example of the well‐known eastern Asian–eastern North American floristic disjunction. The genus consists of three species in eastern Asia, four species in eastern North America, and one species in Central America. Species of the genus are ecologically important trees in eastern North American and eastern Asian forests. The distribution of living species and a rich fossil record of the genus make it an excellent model for understanding the origin and evolution of the eastern Asian–eastern North American floristic disjunction. However, despite the small number of species, relationships within the genus have remained unclear and have not been elucidated using a molecular approach. Here, we integrate data from 48 nuclear genes, fossils, morphology, and ecological niche to resolve species relationships, elucidate its biogeographical history, and investigate the evolution of morphology and ecological niches, aiming at a better understanding of the well‐known EA–ENA floristic disjunction. Results showed that the Central American (CAM)Nyssa talamancanawas sister to the remaining species, which were divided among three, rapidly diversified subclades. Estimated divergence times and biogeographical history suggested thatNyssahad an ancestral range in Eurasia and western North America in the late Paleocene. The rapid diversification occurred in the early Eocene, followed by multiple dispersals between and within the Erasian and North American continents. The genus experienced two major episodes of extinction in the early Oligocene and end of Neogene, respectively. The Central AmericanN. talamancanarepresents a relic lineage of the boreotropical flora in the Paleocene/Eocene boundary that once diversified in western North America. The results supported the importance of both the North Atlantic land bridge and the Bering land bridge (BLB) for the Paleogene dispersals ofNyssaand the Neogene dispersals, respectively, as well as the role of Central America as refugia of the Paleogene flora. The total‐evidence‐based dated phylogeny suggested that the pattern of macroevolution ofNyssacoincided with paleoclimatic changes. We found a number of evolutionary changes in morphology (including wood anatomy and leaf traits) and ecological niches (precipitation and temperature) between the EA–ENA disjunct, supporting the ecological selection driving trait evolutions after geographic isolation. We also demonstrated challenges in phylogenomic studies of lineages with rapid diversification histories. The concatenation of gene data can lead to inference of strongly supported relationships incongruent with the species tree. However, conflicts in gene genealogies did not seem to impose a strong effect on divergence time dating in our case. Furthermore, we demonstrated that rapid diversification events may not be recovered in the divergence time dating analysis using BEAST if critical fossil constraints of the relevant nodes are not available. Our study provides an example of complex bidirectional exchanges of plants between Eurasia and North America in the Paleogene, but “out of Asia” migrations in the Neogene, to explain the present disjunct distribution ofNyssain EA and ENA.

     
    more » « less
  4. Abstract Background and Aims

    Cork oaks (Quercus section Cerris) comprise 15 extant species in Eurasia. Despite being a small clade, they display a range of leaf morphologies comparable to the largest sections (>100 spp.) in Quercus. Their fossil record extends back to the Eocene. Here, we explore how cork oaks achieved their modern ranges and how legacy effects might explain niche evolution in modern species of section Cerris and its sister section Ilex, the holly oaks.

    Methods

    We inferred a dated phylogeny for cork and holly oaks using a reduced-representation next-generation sequencing method, restriction site-associated DNA sequencing (RAD-seq), and used D-statistics to investigate gene flow hypotheses. We estimated divergence times using a fossilized birth–death model calibrated with 47 fossils. We used Köppen profiles, selected bioclimatic parameters and forest biomes occupied by modern species to infer ancestral climatic and biotic niches.

    Key Results

    East Asian and Western Eurasian cork oaks diverged initially in the Eocene. Subsequently, four Western Eurasian lineages (subsections) differentiated during the Oligocene and Miocene. Evolution of leaf size, form and texture was correlated, in part, with multiple transitions from ancestral humid temperate climates to mediterranean, arid and continental climates. Distantly related but ecologically similar species converged on similar leaf traits in the process.

    Conclusions

    Originating in temperate (frost-free) biomes, Eocene to Oligocene ranges of the primarily deciduous cork oaks were restricted to higher latitudes (Siberia to north of Paratethys). Members of the evergreen holly oaks (section Ilex) also originated in temperate biomes but migrated southwards and south-westwards into then-(sub)tropical southern China and south-eastern Tibet during the Eocene, then westwards along existing pre-Himalayan mountain ranges. Divergent biogeographical histories and deep-time phylogenetic legacies (in cold and drought tolerance, nutrient storage and fire resistance) thus account for the modern species mosaic of Western Eurasian oak communities, which are composed of oaks belonging to four sections.

     
    more » « less
  5. null (Ed.)
    The Chicxulub impact crater, on the Yucatán Peninsula of México, is unique. It is the only known terrestrial impact structure that has been directly linked to a mass extinction event and the only terrestrial impact with a global ejecta layer. Of the three largest impact structures on Earth, Chicxulub is the best preserved. Chicxulub is also the only known terrestrial impact structure with an intact, unequivocal topographic peak ring. Chicxulub’s role in the Cretaceous/Paleogene (K-Pg) mass extinction and its exceptional state of preservation make it an important natural laboratory for the study of both large impact crater formation on Earth and other planets and the effects of large impacts on the Earth’s environment and ecology. Our understanding of the impact process is far from complete, and despite more than 30 years of intense debate, we are still striving to answer the question as to why this impact was so catastrophic. During International Ocean Discovery Program (IODP) and International Continental Scientific Drilling Program (ICDP) Expedition 364, Paleogene sedimentary rocks and lithologies that make up the Chicxulub peak ring were cored to investigate (1) the nature and formational mechanism of peak rings, (2) how rocks are weakened during large impacts, (3) the nature and extent of post-impact hydrothermal circulation, (4) the deep biosphere and habitability of the peak ring, and (5) the recovery of life in a sterile zone. Other key targets included sampling the transition through a rare midlatitude Paleogene sedimentary succession that might include Eocene and Paleocene hyperthermals and/or the Paleocene/Eocene Thermal Maximum (PETM); the composition and character of suevite, impact melt rock, and basement rocks in the peak ring; the sedimentology and stratigraphy of the Paleocene–Eocene Chicxulub impact basin infill; the geo- and thermochronology of the rocks forming the peak ring; and any observations from the core that may help constrain the volume of dust and climatically active gases released into the stratosphere by this impact. Petrophysical properties measurements on the core and wireline logs acquired during Expedition 364 will be used to calibrate geophysical models, including seismic reflection and potential field data, and the integration of all the data will calibrate models for impact crater formation and environmental effects. The drilling directly contributes to IODP Science Plan goals: Climate and Ocean Change: How does Earth’s climate system respond to elevated levels of atmospheric CO2? How resilient is the ocean to chemical perturbations? The Chicxulub impact represents an external forcing event that caused a 75% species level mass extinction. The impact basin may also record key hyperthermals within the Paleogene. Biosphere Frontiers: What are the origin, composition, and global significance of subseafloor communities? What are the limits of life in the subseafloor? How sensitive are ecosystems and biodiversity to environmental change? Impact craters can create habitats for subsurface life, and Chicxulub may provide information on potential habitats for life, including extremophiles, on the early Earth and other planetary bodies. Paleontological and geochemical studies at ground zero will document how large impacts affect ecosystems and biodiversity. Earth Connections/Earth in Motion: What mechanisms control the occurrence of destructive earthquakes, landslides, and tsunami? Drilling into the uplifted rocks that form the peak ring will be used to groundtruth numerical simulations and model impact-generated tsunami, and deposits on top of the peak ring and around the Gulf of México will inform us about earthquakes, landslides, and tsunami generated by Chicxulub. These data will collectively help us understand how impact processes are recorded in the geologic record and their potential hazards. IODP Expedition 364 was a Mission Specific Platform expedition designed to obtain subseabed samples and downhole logging measurements from the post-impact sedimentary succession and the peak ring of the Chicxulub impact crater. A single borehole (Hole M0077A) was drilled into the Chicxulub impact crater on the Yucatán continental shelf, recovering core from 505.70 to 1334.69 meters below seafloor (mbsf) with ~99% core recovery. Downhole logs were acquired for the entire depth of the borehole. 
    more » « less