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A Global Phylogeny of Turtles Reveals a Burst of Climate-Associated Diversification on Continental Margins

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A Global Phylogeny of Turtles Reveals a Burst of Climate-Associated Diversification on Continental Margins A global phylogeny of turtles reveals a burst of climate-associated diversification on continental margins Robert C. Thomsona,1, Phillip Q. Spinksb,c, and H. Bradley Shafferb,c aSchool of Life Sciences, University of Hawaiʻi, Honolulu, HI 96822; bDepartment of Ecology and Evolutionary Biology, University of California, Los Angeles, CA 90095; and cLa Kretz Center for California Conservation Science, Institute of the Environment and Sustainability, University of California, Los Angeles, CA 90095 Edited by David B. Wake, University of California, Berkeley, CA, and approved December 30, 2020 (received for review June 12, 2020) Living turtles are characterized by extraordinarily low species diversity built up suggests that turtles may have undergone a diversity given their age. The clade’s extensive fossil record indi- rapid, early adaptive radiation (10). However, this early diver- cates that climate and biogeography may have played important sification was not sustained, and living turtle diversity is low (348 roles in determining their diversity. We investigated this hypoth- extant species; ref. 11). Testudine diversity is strikingly depau- esis by collecting a molecular dataset for 591 individual turtles perate relative to other, much younger crown amniote clades that, together, represent 80% of all turtle species, including rep- such as birds (>10,000 species with a crown age 111 mya), resentatives of all families and 98% of genera, and used it to mammals (>5,000 species, 177 mya), and squamate reptiles jointly estimate phylogeny and divergence times. We found that (>10,000 species, 201 mya; refs. 12–15). the turtle tree is characterized by relatively constant diversifica- At present, turtles are also one of the most endangered clades tion (speciation minus extinction) punctuated by a single threefold of vertebrates on the planet. More than one-third of chelonian increase. We also found that this shift is temporally and geograph- species fall in the International Union for Conservation of Na- ically associated with newly emerged continental margins that ture (IUCN) Endangered, Critically Endangered, or Extinct appeared during the Eocene−Oligocene transition about 30 mil- categories, and more than three-quarters of species are at serious lion years before present. In apparent contrast, the fossil record risk (IUCN Red List categories of Near Threatened, Vulnerable, EVOLUTION from this time period contains evidence for a major, but regional, or greater; see ref. 12). In addition to well-documented losses extinction event. These seemingly discordant findings appear to from human exploitation, several novel, climate-associated con- be driven by a common global process: global cooling and drying servation challenges have recently emerged, ranging from in- at the time of the Eocene−Oligocene transition. This climatic shift creasing incursions of sea water into freshwater habitats (16), to led to aridification that drove extinctions in important fossil- sex ratio shifts associated with temperature-dependent sex de- bearing areas, while simultaneously exposing new continental termination that most turtles employ (17), to the wholesale loss margin habitat that subsequently allowed for a burst of speciation of critical nesting areas (18). associated with these newly exploitable ecological opportunities. Thus, from both macroevolutionary and conservation biology perspectives, turtles represent a biodiversity conundrum. As a turtle tree of life | divergence time estimation | GeoSSE | HiSSE | global lineage, they are long lived, and morphologically and ecologically climate change Significance lobal patterns of species diversity vary markedly across Gsegments of the tree of life. Environmental changes, across Biodiversity is unevenly distributed across the tree of life. Un- spatial and temporal scales, are expected to influence patterns of derstanding the factors that led to this unevenness can illu- species richness and distribution, and documenting these mac- minate how macroevolutionary processes have interacted with roevolutionary effects can aid our understanding of historical changing global environments to shape patterns of biodiver- and current environmental impacts on biodiversity (1). This is sity. By developing a comprehensive phylogeny for extant particularly important for clades of high conservation concern turtles and analyzing the diversification dynamics of the group, that are declining due to human-mediated climate change. While we show that species-level diversity is strongly associated with conservation actions for these clades must necessarily operate on historical climate shifts. Our findings indicate that newly ex- local scales to protect individual species, a more global under- posed continental margins created during a period of cooling standing of how past climate changes have impacted their bio- and drying are important evolutionary cradles for turtle spe- diversity may inform more coordinated management efforts in a ciation, explain why turtle biodiversity is orders of magnitude rapidly advancing Anthropocene. more depauperate than the remaining major lineages of am- Turtles (Testudines) are an evolutionarily unique and mor- niotes, and reconcile the seemingly contradictory insights that phologically distinctive clade of vertebrates that are imperiled on fossils and extant species suggest into a single picture of a global scale (2, 3). Characterized by the presence of a bony evolutionary diversification. carapace and plastron that house both the pectoral and pelvic girdles, turtles possess one of the most derived tetrapod mor- Author contributions: R.C.T., P.Q.S., and H.B.S. designed research; R.C.T., P.Q.S., and H.B.S. phologies known. They are also an ancient clade, with stem performed research; R.C.T. and P.Q.S. analyzed data; and R.C.T., P.Q.S., and H.B.S. wrote fossils dating to the Late Permian or Triassic and a crown age the paper. estimated at 220 million years ago (mya) (4–6). Turtles enjoy an The authors declare no competing interest. essentially global distribution spanning an ecologically diverse This article is a PNAS Direct Submission. set of terrestrial, marine, and freshwater habitats, and have in- Published under the PNAS license. vaded each multiple times during their long history (7, 8). 1To whom correspondence may be addressed. Email: [email protected]. After they appear in the fossil record near the time of the This article contains supporting information online at https://www.pnas.org/lookup/suppl/ earliest dinosaurs, testudines rapidly expanded in geographic doi:10.1073/pnas.2012215118/-/DCSupplemental. range and ecological diversity (6, 9). The speed with which this Published February 8, 2021. PNAS 2021 Vol. 118 No. 7 e2012215118 https://doi.org/10.1073/pnas.2012215118 | 1of10 Downloaded by guest on September 25, 2021 conservative, suggesting evolutionary resilience. However, their drivers of these patterns are not well understood, and potentially low species richness and high degree of endangerment point to operate differentially depending on geographic scale and context. the fragility of the lineage in the human-dominated Anthro- To better understand these processes, we investigated the pocene, rendering them an important conservation target. Un- global diversification history of turtles using molecular phylo- derstanding the history of diversification responsible for the genetic data. To do so, we developed a well-sampled, nearly modern diversity of turtles may hold important clues to their complete phylogeny for the world’s extant turtles and used it to future survival, but has been hindered by the lack of a robust, estimate divergence times and quantify the temporal and geo- well-sampled, time-calibrated phylogeny. A growing number of graphic patterns of diversification that gave rise to present-day molecular phylogenetic studies have targeted the deep family- diversity. We found relatively steady rates of diversification level relationships within the group (5, 19–24), or more narrowly throughout most of the group’s history, followed by a sharp in- focused within-family or within-genus relationships with more crease in diversification rates within the last 50 million years that complete species level sampling (25–42). Despite these efforts, a coincides with a long period of global cooling, large scale sea well-sampled multilocus phylogeny for the clade has remained level declines (>100 m), and the consequent availability of ex- elusive, in large part because of the difficulty of obtaining tissue tensive, previously unavailable habitat. These rate increases are samples from the many rare/endangered taxa. Several studies geographically concentrated along coastal margins and low-lying have assembled existing data from GenBank to increase the areas that were exposed as sea levels fell, suggesting that climate number of species included in a tree. While informative, this change has been an important driver in patterns of both local approach necessarily comes with the cost of large blocks of extinction and speciation during the evolution of turtles. missing data which can decrease accuracy in estimates of both Results and Discussion phylogeny and divergence times (43–46). As a consequence, studies of turtle diversification have largely focused on limited Phylogeny. We developed a well-sampled phylogenetic hypothesis geographic, taxonomic, or temporal scales, with little synthesis of for the extant Testudines. Our taxon sampling includes all 14 the global evolutionary mechanisms
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