Abstract
The carnivorous plant family Sarraceniaceae comprises three genera of wetland-inhabiting pitcher plants: Darlingtonia in the northwestern United States, Sarracenia in eastern North America, and Heliamphora in northern South America. Hypotheses concerning the biogeographic history leading to this unusual disjunct distribution are controversial, in part because genus- and species-level phylogenies have not been clearly resolved. Here, we present a robust, species-rich phylogeny of Sarraceniaceae based on seven mitochondrial, nuclear, and plastid loci, which we use to illuminate this family's phylogenetic and biogeographic history. The family and genera are monophyletic: Darlingtonia is sister to a clade consisting of Heliamphora+Sarracenia. Within Sarracenia, two clades were strongly supported: one consisting of S. purpurea, its subspecies, and S. rosea; the other consisting of nine species endemic to the southeastern United States. Divergence time estimates revealed that stem group Sarraceniaceae likely originated in South America 44–53 million years ago (Mya) (highest posterior density [HPD] estimate = 47 Mya). By 25–44 (HPD = 35) Mya, crown-group Sarraceniaceae appears to have been widespread across North and South America, and Darlingtonia (western North America) had diverged from Heliamphora+Sarracenia (eastern North America+South America). This disjunction and apparent range contraction is consistent with late Eocene cooling and aridification, which may have severed the continuity of Sarraceniaceae across much of North America. Sarracenia and Heliamphora subsequently diverged in the late Oligocene, 14–32 (HPD = 23) Mya, perhaps when direct overland continuity between North and South America became reduced. Initial diversification of South American Heliamphora began at least 8 Mya, but diversification of Sarracenia was more recent (2–7, HPD = 4 Mya); the bulk of southeastern United States Sarracenia originated co-incident with Pleistocene glaciation, <3 Mya. Overall, these results suggest climatic change at different temporal and spatial scales in part shaped the distribution and diversity of this carnivorous plant clade.
Highlights
Carnivory has evolved at least six times within the flowering plants [1,2] and is thought to be an adaption to increase the uptake of nitrogen and phosphorous in the nutrient-poor, aquatic and wetland environments where these plants grow [3,4]
Within Sarraceniaceae, Heliamphora always emerged as sister to Sarracenia (Figs. 2, 3)
Our biogeographic analyses reveal that stem-group Sarraceniaceae originated in South America 44– 53 million years ago (Mya), and that by 25–44 Mya, crown-group Sarraceniaceae had achieved a widespread distribution across South and North America (Fig. 4A)
Summary
Carnivory has evolved at least six times within the flowering plants [1,2] and is thought to be an adaption to increase the uptake of nitrogen and phosphorous in the nutrient-poor, aquatic and wetland environments where these plants grow [3,4]. We present the most fully-resolved phylogeny of the American pitcher-plant family Sarraceniaceae to date. We use these data to estimate molecular divergence times of the group and to address a long-standing debate on the biogeographic origin and the disjunct distribution of these three genera. Some carnivorous plant families, such as the Cephalotaceae, Roridulaceae, and Byblidaceae, are endemics occurring on single (sub)continents, whereas others, such as Droseraceae and Lentibulariaceae have cosmopolitan distributions [1,2,5,6,7,8,9,10,11]. The enigmatic, disjunct distribution of the three genera of the American pitcher plants, Sarraceniaceae (Fig. 1), presents an unresolved question for botanists, biogeographers, and evolutionary biologists. Sarraceniaceae itself is a well-supported member of the Ericales [2,12,13,14,15], and is distinguished from other close relatives by its modified pitcherlike leaves [16] that trap and digest arthropod prey [17], and nodding, bisexual flowers [14] that are pollinated by a variety of bees and flies [18,19,20]
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