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Phylogenetic Relationships of Polemoniaceae: Inferences from Mitochondrial Nad1b Intron Sequences J Aliso: A Journal of Systematic and Evolutionary Botany Volume 17 | Issue 2 Article 6 1998 Phylogenetic Relationships of Polemoniaceae: Inferences From Mitochondrial Nad1b Intron Sequences J. Mark Porter Rancho Santa Ana Botanic Garden Leigh A. Johnson North Carolina State University Follow this and additional works at: http://scholarship.claremont.edu/aliso Part of the Botany Commons Recommended Citation Porter, J. Mark and Johnson, Leigh A. (1998) "Phylogenetic Relationships of Polemoniaceae: Inferences From Mitochondrial Nad1b Intron Sequences," Aliso: A Journal of Systematic and Evolutionary Botany: Vol. 17: Iss. 2, Article 6. Available at: http://scholarship.claremont.edu/aliso/vol17/iss2/6 Aliso. 17(2), pp. 157-188 © 1998, by The Rancho Santa Ana Botanic Garden, Claremont, CA 91711-3157 PHYLOGENETIC RELATIONSHIPS OF POLEMONIACEAE: INFERENCES FROM MITOCHONDRIAL NAD1B INTRON SEQUENCES J. MARK PORTER Rancho Santa Ana Botanic Garden 1500 North College Ave Claremont, CA 91711-3422 e-mail: [email protected] AND LEIGH A. JOHNSON Department of Botany Box 7612 North Carolina State University Raleigh, NC 27695-7612 ABSTRACT The most recent assessments of phylogenetic relationships and diversification in the flowering plant family Polemoniaceae have relied on nuclear ribosomal and chloroplast DNA sequences. We employed the mitochondrial nadl b intron, located within the second transcription unit of the first subunit of NADH dehydrogenase, for phylogenetic inference. Maximum parsimony analysis of these data pro­ vided evidence that Polemoniaceae are more closely related to families Fouquieriaceae, Diapensiaceae, Styracaceae, and Primulaceae than to families of the Solananae, where it has been classified. Fou­ quieriaceae are inferred to be the sister group of Polemoniaceae; however, when indels are treated as additional characters and given twice the weight of a nucleotide substitution the sister group of Po­ lemoniaceae is a clade that includes Fouquieriaceae, Diapensiaceae, and Primulaceae. Mitochondrial DNA sequences also provided support for an early diversification of Polemoniaceae involving three lineages: the Acanthogilia lineage, the Cobaea-Cantua-Bonplandia lineage, and a lineage including the remaining sampled genera of the family. These results are highly consistent with phylogenetic estimates based on chloroplast and nuclear gene sequences. However, because the exact branch order is not known with confidence for these three lineages, nor are the closest relatives to Polemoniaceae, assessments of homology in morphological characters remains tenuous. For example, both Fouquier­ iaceae and Acanthogilia possess primary leaves that become persistent spines. It was shown that, in spite of the morphological similarity, spiny primary leaves in Fouquieriaceae and Polemoniaceae are not homologous. Key words: Polemoniaceae, mitochondrial nadl b intron sequences, phylogenetics, systematics. INTRODUCTION the southwestern United States. Recently, DNA se­ quence analyses of chloroplast and nuclear genes have Polemoniaceae are a familiar component of the flora been used to assess and clarify phylogenetic relation­ of the southwestern United States and northern Mexico ships for this family to provide a more reliable frame­ where, as noted by Mason and Day (1948), local and work for ecological and evolutionary studies (Steele seasonal climatic variation superimposed over geo­ and Vilgalys 1994; Johnson et al. 1996, 1998 in press; graphic and edaphic variables provide these regions Porter 1996). Novel insights into affinities among taxa with a tremendous diversity of habitats and ecological and confidence limits on suggested relationships have niches. Polemoniaceae represent one of several fami­ been provided by these investigations. However, it is lies that have exploited this varied environment, as ev­ readily apparent that several important relationships idenced by high levels of regional endemism and the pertaining to the early diversification of the family re­ great diversity of genera and species existing in the main unclear. Principal among these are the branching floristic regions of the Southwest (Grant 1959). The pattern among the primary lineages within the family combination of rich diversity in ecological preferences, and the precise sister group affinities for the family as morphology, and breeding systems, has contributed to a whole-relationships that have been enigmatic his­ the use of Polemoniaceae as a model for investigating torically as well. patterns and processes of diversification in the flora of For the last century Polemoniaceae have been con- 158 Porter and Johnson ALISO sidered a "natural group" (Grant 1959). However, morphy with some Theanae families, carpel number, Linnaeus (1737) placed portions of the family near is ambiguously scored although the rare deviations Convolvulus and Campanula while other parts were from tricarpelly in Polemoniaceae are clearly derived). placed near Diapensia and Azalea. It was not until the Neither analysis included measures of support; our treatments of Persoon (1805) and deJussieu (1810) that own reanalyses of both data sets show that the addition most genera currently included in the family were clas­ of only 1 step to the most parsimonious tree length of sified together. Even so, there remained controversy both data sets is required to position Polemoniaceae regarding the inclusion of Cobaea in Polemoniaceae variously among other taxa. Consequently, current (Persoon 1805; deJussieu 1810; D. Don 1822, 1824; quantitative phylogenetic approaches employing mor­ G. Don 1838). Following the work of Bentham (1845), phological evidence provide little additional insight most authors have included Cobaea within Polemon­ into the placement of Polemoniaceae beyond showing iaceae (but see Dahlgren 1980). In addition, several that a close relationships with Convolvulaceae, Sola­ genera not currently included in Polemoniaceae, were naceae, and Hydrophyllaceae are not unambiguously periodically included, prior to the treatment of Ben­ supported. tham (1845). Particularly relevant to the present study Phylogenetic relationships of Polemoniaceae sug­ are the genera Diapensia, included in Polemoniaceae gested by molecular data have consistently been at by Ventenat (1794) and G . Don (1838), and Fouquier­ odds with modern classifications (e.g., Cronquist 1981; ia, the first described species of which was included Thorne 1992; Takhtajan 1997). Protein sequences of in the genus Cantua of Polemoniaceae (i.e., Cantua the nuclear encoded small subunit of ribulose-l ,5-bis­ Jasciculata Willd. ex Roem. & Schult.). phosphate carboxylase/oxygenase (rbcS) provide evi­ Like many flowering plant families, inferred rela­ dence that supports the placement of Polemoniaceae tionships of Polemoniaceae with other families have away from Solanaceae and Hydrophyllaceae (Martin varied from author to author, but a recurring pattern and Dowd 1991). The rbcS data support Polemoni­ of suggested affinities is evident. Historically, Pole­ aceae (not unambiguously a monophyletic group!) moniaceae have been most frequently aligned with placed within a clade that includes Ericaceae, Epacri­ Convolvulaceae (e.g., deJussieu 1789) or Solanaceae daceae, and Convolvulaceae. Chloroplast restriction and Hydrophyllaceae (e.g., Bartling 1830). However, site data (Downie and Palmer 1992) similarly suggest various authors have suggested relationships with Polemoniaceae are not closely related to Solanaceae many disparate families, including Primulaceae (Hal­ and Hydrophyllaceae; however, this analysis also sep­ lier 1905; Bessey 1915), Ericaceae (Brown 1938), and arates Polemoniaceae from Convolvulaceae, the for­ Fouquieriaceae (Engler and Gilg 1924; Flory 1937; mer being placed with Fouquieriaceae as the sister Abrams 1951). Most recent classifications of flowering group of a clade that includes families of Asteranae plants continue to ally Polemoniaceae with Convol­ and Solananae. Sequences of the chloroplast gene rbcL vulaceae, Solanaceae, and Hydrophyllaceae (Grant (large subunit of ribulose-l,5-bisphosphate carboxyl­ 1959; Dahlgren 1980; Cronquist 1981; Thorne 1992; ase/oxygenase) likewise provide evidence for relation­ Takhtajan 1997). ships between Polemoniaceae and Theanae families Cladistic analyses of morphological data have thus (including Fouquieriaceae), while also suggesting that far not provided a consistent, unambiguous picture of Solanaceae, Hydrophyllaceae, and Convolvulaceae are relationships between Polemoniaceae and other flow­ only distantly related (Olmstead et al. 1992, 1993; ering plant families. Hufford's (1992) study of the re­ Chase et al. 1993; Morton et al. 1997). Taxon sampling lationships of Rosidae to other families found Pole­ between the various rbcL analyses varies and, as a moniaceae sharing most recent common ancestry with result, the inferred sister group relationship of Pole­ Pittosporaceae. When in a clade with Pittosporaceae, moniaceae also varies. Sequences of the chloroplast Polemoniaceae are depicted as the sister group to fam­ gene matK also provide evidence that Polemoniaceae ilies of the Asteranae and Solananae (but not Theanae). are more closely related to Theanae (ericalean) fami­ Hufford noted, however, many traits shared by Pole­ lies and Fouquieriaceae, than to Solanaceae (Johnson moniaceae and some Theanae families (e.g., Erica­ et al. 1996). More recently, analysis of nuclear encod­ ceae), including tricarpellate gynoecia, loculicidal cap­ ed 18S ribosomal DNA sequences
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