Linnaeus's folly – phylogeny, evolution and classification of Sedum (Crassulaceae) and Crassulaceae subfamily Sempervivoideae

Abstract

Sedum, containing approximately 470 species, is by far the largest genus of Crassulaceae. Three decades of molecular phylogenetic work have provided evidence for the non‐monophyly of Sedum and many more of the 30 genera of Crassulaceae subfam. Sempervivoideae. In this study, we present a broadly sampled and dated molecular phylogeny of Sempervivoideae including 80% of all infrageneric taxa described in Sedum as well as most other genera of the subfamily. We used sequences of one nuclear (ITS) and three plastid markers (matK, rps16, trnL‐trnF). The five major lineages of Sempervivoideae (i.e., Telephium clade, Petrosedum clade, Sempervivum/Jovibarba, Aeonium clade, Leucosedum plus Acre clades) were resolved as successive sister to each other in the phylogenetic analysis of the plastid markers, while in the ITS phylogeny the Petrosedum clade is the closest relative of the Aeonium clade. Our dating analysis of ITS suggests that Sempervivoideae diversified rapidly throughout the Paleocene and Eocene, possibly in the area of the former Tethys and Paratethys archipelago. A biogeographic pattern emerges in which migration out of this ancestral area is linked to pronounced morphological evolution resulting in several distinct lineages recognized as segregate genera thought to be derived from Sedum. These segregate genera, however, have been defined on the basis of strongly homoplasious characters such as degree of petal fusion, petal colouration or flower merism. Moreover, all character states currently used for the delimitation of segregate genera seem to be homoplasious, and each of them can be found in at least one species of Sedum. Extensive literature work led to the conclusion that only few of the monophyletic clades found by us can be defined unambiguously by morphological characters. Mainly for these two reasons, we believe that combination of all 14 genera currently recognized in tribe Sedeae (= clades Leucosedum plus Acre) into Sedum might be the most stable solution of the “Sedum problem”. This new Sedum s.l. would then comprise approximately 755 species.

The Conservation of Chloroplast Genome Structure and Improved Resolution of Infrafamilial Relationships of Crassulaceae

“…Moreover, phylogenetic studies of Crassulaceae have relied primarily on a limited set of chloroplast markers (e.g., matK, rps16, and trnL-trnF). Our comparative analyses, however, have shown that these chloroplast markers appear to be relatively low in nucleotide diversity (Figure 2), which may be partially responsible for the lack of phylogenetic resolution within Sempervivoideae (Mort et al, 2001;Messerschmid et al, 2020). Thus, to achieve better phylogenetic resolution, future studies of Crassulaceae should focus on molecular markers from more variable regions of the chloroplast genome, such as ccsA-ndhD, rps16-trnQ, rpl32-trnL, and trnH-psbA (Prince, 2015).…”

“…The angiosperm family Crassulaceae, also known as the stonecrop family, belongs to the order Saxifragales and include 34 genera and approximately 1,400 species (APG IV, 2016;Messerschmid et al, 2020), which are predominantly perennial herbs, subshrubs, or shrubs (Thiede and Eggli, 2007). The species of Crassulaceae primarily occur in (semi-)arid and mountainous habitats of the temperate and subtropical areas (van Ham and Hart, 1998), and are distributed worldwide with centers of diversity in Mexico, southern Africa, Macaronesia, and the Himalayas (Mort et al, 2001).…”

“…The largest and most complex subfamily Sempervivoideae contain 28 genera and over 1,000 species (Thiede and Eggli, 2007), and the inter-and intrageneric relationships have been investigated by a considerable number of studies (e.g., Mes et al, 1997;Jorgensen and Frydenberg, 1999;Mort et al, 2002;Acevedo-Rosas et al, 2004;Fairfield et al, 2004;Mayuzumi and Ohba, 2004;Gontcharova et al, 2006;Carrillo-Reyes et al, 2008Yost et al, 2013;Zhang et al, 2014;Klein and Kadereit, 2015;Nikulin et al, 2016;Vázquez-Cotero et al, 2017;de la Cruz-López et al, 2019). These phylogenetic studies have led to the recognition of five tribes within Sempervivoideae by Thiede and Eggli (2007) (Messerschmid et al, 2020). Despite the significant progress made in the tribal and generic circumscription of Crassulaceae, phylogenetic relationships among tribes and major clades remain poorly to moderately supported or sometimes contradicted, especially within Sempervivoideae (Supplementary Figure 1).…”

“…Until now, numerous phylogenetic studies have been performed to evaluate the infrafamilial relationships of Crassulaceae with a broad taxon sampling (e.g., Berger, 1930 ; van Ham and Hart, 1998 ; Mort et al, 2001 ; Mayuzumi and Ohba, 2004 ; Gontcharova et al, 2006 , 2008 ; Folk et al, 2019 ; Messerschmid et al, 2020 ), which have led to the establishment of three subfamilies by Thiede and Eggli (2007) , i.e., Crassuloideae, Kalanchoideae, and Sempervivoideae. Although most of these studies are based on one or a few genetic loci, the monophyly of each of three subfamilies sensu Thiede and Eggli (2007) is well supported.…”

“…The inter- and intrageneric relationships within each of three subfamilies have been also extensively studied using a variety of chloroplast and nuclear loci. The smallest subfamily Crassuloideae comprise approximately 200 species in a single genus, Crassula L. ( Messerschmid et al, 2020 ), whose intrageneric relationships have been recently addressed by sampling 103 species ( Bruyns et al, 2019 ). The subfamily Kalanchoideae include approximately 240 species in four genera ( Smith et al, 2019 ), i.e., Adromischus Lem., Cotyledon L., Kalanchoe , and Tylecodon Toelken, and the inter- and intrageneric relationships have been exclusively assessed in a few separate studies ( Gehrig et al, 2001 ; Mort et al, 2005 ; Nowell, 2008 ).…”