INTRODUCTION Resolving the role that different environmental forces may have played in the apparent explosive diversification of modern placental mammals is crucial to understanding the evolutionary context of their living and extinct morphological and genomic diversity. RATIONALE Limited access to whole-genome sequence alignments that sample living mammalian biodiversity has hampered phylogenomic inference, which until now has been limited to relatively small, highly constrained sequence matrices often representing <2% of a typical mammalian genome. To eliminate this sampling bias, we used an alignment of 241 whole genomes to comprehensively identify and rigorously analyze noncoding, neutrally evolving sequence variation in coalescent and concatenation-based phylogenetic frameworks. These analyses were followed by validation with multiple classes of phylogenetically informative structural variation. This approach enabled the generation of a robust time tree for placental mammals that evaluated age variation across hundreds of genomic loci that are not restricted by protein coding annotations. RESULTS Coalescent and concatenation phylogenies inferred from multiple treatments of the data were highly congruent, including support for higher-level taxonomic groupings that unite primates+colugos with treeshrews (Euarchonta), bats+cetartiodactyls+perissodactyls+carnivorans+pangolins (Scrotifera), all scrotiferans excluding bats (Fereuungulata), and carnivorans+pangolins with perissodactyls (Zooamata). However, because these approaches infer a single best tree, they mask signatures of phylogenetic conflict that result from incomplete lineage sorting and historical hybridization. Accordingly, we also inferred phylogenies from thousands of noncoding loci distributed across chromosomes with historically contrasting recombination rates. Throughout the radiation of modern orders (such as rodents, primates, bats, and carnivores), we observed notable differences between locus trees inferred from the autosomes and the X chromosome, a pattern typical of speciation with gene flow. We show that in many cases, previously controversial phylogenetic relationships can be reconciled by examining the distribution of conflicting phylogenetic signals along chromosomes with variable historical recombination rates. Lineage divergence time estimates were notably uniform across genomic loci and robust to extensive sensitivity analyses in which the underlying data, fossil constraints, and clock models were varied. The earliest branching events in the placental phylogeny coincide with the breakup of continental landmasses and rising sea levels in the Late Cretaceous. This signature of allopatric speciation is congruent with the low genomic conflict inferred for most superordinal relationships. By contrast, we observed a second pulse of diversification immediately after the Cretaceous-Paleogene (K-Pg) extinction event superimposed on an episode of rapid land emergence. Greater geographic continuity coupled with tumultuous climatic changes and increased ecological landscape at this time provided enhanced opportunities for mammalian diversification, as depicted in the fossil record. These observations dovetail with increased phylogenetic conflict observed within clades that diversified in the Cenozoic. CONCLUSION Our genome-wide analysis of multiple classes of sequence variation provides the most comprehensive assessment of placental mammal phylogeny, resolves controversial relationships, and clarifies the timing of mammalian diversification. We propose that the combination of Cretaceous continental fragmentation and lineage isolation, followed by the direct and indirect effects of the K-Pg extinction at a time of rapid land emergence, synergistically contributed to the accelerated diversification rate of placental mammals during the early Cenozoic. The timing of placental mammal evolution. Superordinal mammalian diversification took place in the Cretaceous during periods of continental fragmentation and sea level rise with little phylogenomic discordance (pie charts: left, autosomes; right, X chromosome), which is consistent with allopatric speciation. By contrast, the Paleogene hosted intraordinal diversification in the aftermath of the K-Pg mass extinction event, when clades exhibited higher phylogenomic discordance consistent with speciation with gene flow and incomplete lineage sorting.
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West Indian Mammals The Old, the New, and the Recently Extinct
The West Indian mammal fauna has played a key role in the development of biogeographic ideas for over a century, but a synthesis explaining regional patterns of mammal diversity and distribution in a historical framework has not emerged. We review recent phylogenetic, population genetic, and radiocarbon dating studies of West Indian mammals and explore the biological and historical drivers of colonization, speciation, and extinction in this region of endemism. We also present the first complete list of all its extant and extinct mammals. The mammalian biota is older than was earlier presumed, with many ancient endemic lineages, even among highly vagile organisms such as bats. Land bridges, Cenozoic eustatic sea-level changes, and Pleistocene glacial cycles have been proposed to explain the colonization of the islands, but phylogenetic divergence analyses often conlict with the timing of these events and favor alternative biogeographic histories. The loss of West Indian biodiversity is incompletely understood, but new radiometric chronologies indicate that anthropogenic impacts rather than glacial-interglacial environmental changes are responsible for most Quaternary extinction and extirpation events involving land mammals. However, many outstanding questions of historical biogeography remain unresolved, including appropriate methods for interpreting phylogenies and divergence estimates in a biogeographic context, and whether to use vicariance or dispersal as the null hypothesis when investigating regional patterns of colonization, speciation, and extinction in comparative analyses. We propose synthetic approaches drawing from phylogenetics, population genetics, paleogeography, paleontology, and even archaeology to resolve persisting questions in Caribbean biogeography.
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- Award ID(s):
- 0949759
- NSF-PAR ID:
- 10017046
- Date Published:
- Journal Name:
- Bones, Clones, and Biomes: An Extended History of Recent Neotropical Mammals
- Page Range / eLocation ID:
- 157-202
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Aim Tropical regions harbour over half of the world's mammals and birds, but how their communities have assembled over evolutionary timescales remains unclear. To compare eco‐evolutionary assembly processes between tropical mammals and birds, we tested how hypotheses concerning niche conservatism, environmental stability, environmental heterogeneity and time‐for‐speciation relate to tropical vertebrate community phylogenetic and functional structure.
Location Tropical rainforests worldwide.
Time period Present.
Major taxa studied Ground‐dwelling and ground‐visiting mammals and birds.
Methods We used in situ observations of species identified from systematic camera trap sampling as realized communities from 15 protected tropical rainforests in four tropical regions worldwide. We quantified standardized phylogenetic and functional structure for each community and estimated the multi‐trait phylogenetic signal (PS) in ecological strategies for the four regional species pools of mammals and birds. Using linear regression models, we test three non‐mutually exclusive hypotheses by comparing the relative importance of colonization time, palaeo‐environmental changes in temperature and land cover since 3.3 Mya, contemporary seasonality in temperature and productivity and environmental heterogeneity for predicting community phylogenetic and functional structure.
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Location Western North America.
Taxon Western terrestrial garter snake,
Thamnophis elegans .Methods We used double‐digest RADseq to estimate phylogenetic relationships and characterize population genetic structure across the three widespread subspecies of
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Abstract The complex island archipelagoes of Wallacea and Melanesia have provided empirical data behind integral theories in evolutionary biology, including allopatric speciation and island biogeography. Yet, questions regarding the relative impact of the layered biogeographic barriers, such as deep-water trenches and isolated island systems, on faunal diversification remain underexplored. One such barrier is Wallace’s Line, a significant biogeographic boundary that largely separates Australian and Asian biodiversity. To assess the relative roles of biogeographic barriers—specifically isolated island systems and Wallace’s Line—we investigated the tempo and mode of diversification in a diverse avian radiation, Corvides (Crows and Jays, Birds-of-paradise, Vangas, and allies). We combined a genus-level data set of thousands of ultraconserved elements (UCEs) and a species-level, 12-gene Sanger sequence matrix to produce a well-resolved supermatrix tree that we leveraged to explore the group’s historical biogeography and the effects of the biogeographic barriers on their macroevolutionary dynamics. The tree is well resolved and differs substantially from what has been used extensively for past comparative analyses within this group. We confirmed that Corvides, and its major constituent clades, arose in Australia and that a burst of dispersals west across Wallace’s Line occurred after the uplift of Wallacea during the mid-Miocene. We found that dispersal across this biogeographic barrier was generally rare, though westward dispersals were two times more frequent than eastward dispersals. Wallacea’s central position between Sundaland and Sahul no doubt acted as a bridge for island-hopping dispersal out of Australia, across Wallace’s Line, to colonize the rest of Earth. In addition, we found that the complex island archipelagoes east of Wallace’s Line harbor the highest rates of net diversification and are a substantial source of colonists to continental systems on both sides of this biogeographic barrier. Our results support emerging evidence that island systems, particularly the geologically complex archipelagoes of the Indo-pacific, are drivers of species diversification. [Historical biogeography; island biogeography; Melanesia; molecular phylogenetics; state-dependent diversification and extinction.]
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Accepted Manuscript1.0
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