1 Relationships of Angiosperms To

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1 Relationships of Angiosperms To Relationships of Angiosperms to 1 Other Seed Plants Seed plants are of fundamental importance both evolution- all gymnosperms (living and extinct) together are not arily and ecologically. They dominate terrestrial landscapes, monophyletic. Importantly, several fossil lineages, Cayto- and the seed has played a central role in agriculture and hu- niales, Bennettitales, Pentoxylales, and Glossopteridales man history. There are fi ve extant lineages of seed plants: (glossopterids), have been proposed as putative close rela- angiosperms, cycads, conifers, gnetophytes, and Ginkgo. tives of the angiosperms based on phylogenetic analyses These fi ve groups have usually been treated as distinct (e.g., Crane 1985; Rothwell and Serbet 1994; reviewed in phyla — Magnoliophyta (or Anthophyta), Cycadophyta, Doyle 2006, 2008, 2012; Friis et al. 2011). These fossil lin- Co ni fe ro phyta, Gnetophyta, and Ginkgophyta, respec- eages, sometimes referred to as the para-angiophytes, will tively. Cantino et al. (2007) used the following “rank- free” therefore be covered in more detail later in this chapter. An- names (see Chapter 12): Angiospermae, Cycadophyta, other fossil lineage, the corystosperms, has been proposed Coniferae, Gnetophyta, and Ginkgo. Of these, the angio- as a possible angiosperm ancestor as part of the “mostly sperms are by far the most diverse, with ~14,000 genera male hypothesis” (Frohlich and Parker 2000), but as re- and perhaps as many as 350,000 (The Plant List 2010) to viewed here, corystosperms usually do not appear as close 400,000 (Govaerts 2001) species. The conifers, with ap- angiosperm relatives in phylogenetic trees. proximately 70 genera and nearly 600 species, are the sec- The seed plants represent an ancient radiation, with ond largest group of living seed plants. Cycads comprise the fi rst seeds appearing near the end of the Devonian 10 genera and approximately 300 species (Osborne et al. (~370 million years ago; mya). By the Early to Middle Car- 2012; Fragnière et al. 2015). Gnetales consist of three mor- boniferous, a diversity of seed plant lineages already ex- phologically disparate genera, Gnetum, Ephedra, and Wel- isted (e.g., Cordaites and walchian conifers; Thomas 1955; witschia (~90 species total) that are so distinctive that each Bhatnagar and Moitra 1996; Kenrick and Crane 1997; has been placed in its own family (Gnetaceae, Ephedraceae, Davis and Kenrick 2004; T. Taylor et al. 2009). Hetero- and Welwitschiaceae). There is a single living species of spory, prerequisite to evolution of the seed, evolved in par- Ginkgo, G. biloba. Each of these extant lineages has a rich allel in different major clades, including lycophytes, water fossil history (T. Taylor et al. 2009; Friis et al. 2011); we ferns (e.g., Marsilea), sphenophytes, and aneurophytes, and cover the fossil record of the angiosperms in more detail seed- like structures, with a retained endosporic megagame- in Chapter 2 and also in those chapters focused on specifi c tophyte nearly surrounded by an integument-like covering, angiosperm clades (Chapters 4–10). occur in some lycophytes (e.g., Lepidocarpon). Lepidocar- There are also many extinct lineages of seed plants pon is not considered a true seed, but is an example of con- (Crane 1985; Decombeix et al. 2010; E. Taylor and T. Tay- vergence. Importantly, phylogenetic analyses that include lor 2009; T. Taylor et al. 2009). Although extant gymno- the fi ve clades of living seed plants show that they indeed sperms appear to be monophyletic (below and Chapter 2), form a clade, indicating that all have inherited seeds from 2 Chapter 1 a common ancestor— and that these seeds did not evolve in organs, endosperm, vessel elements), may be infl uenced by parallel. Phylogenetic analyses including extinct seed plants those taxa considered their closest relatives. The effect of also place these groups in the same clade as extant seed outgroup choice on the reconstruction of character evo- plants (see below). Thus, analyses support the hypothesis lution within angiosperms is readily seen via the wide- that fossil and extant seed plants (Spermatophyta) had a spread use of Gnetales as an outgroup for angiosperms. single origin. As reviewed below, for nearly two decades beginning in The fi rst seed- like structures, observed in the Late De- the 1980s, Gnetales were considered by many to represent vonian to early Carboniferous, apparently ancestral to true the closest living relatives of the angiosperms. The use of seeds, had free integumentary lobes and lacked a micropyle; Gnetales as an angiosperm outgroup profoundly infl uenced the pollen- receptive structure, lagenostome, was formed character- state reconstruction within the fl owering plants by the nucellus rather than the integument. The fusion of (see “The Anthophyte Hypothesis” section). integumentary lobes, except for a micropylar channel, led Clarifying relationships among seed plants, both extant to the formation of true seeds as in lyginopterid seed ferns. and fossil, has been extremely diffi cult. Factors that have The fossil record of conifers dates to the Late Carbonif- contributed to the diffi culties in phylogeny reconstruc- erous and that of true cycads to the Early Permian. Avail- tion of seed plants (living and extinct) include the great able data indicate that by the Permian (~299–251 mya), age of these groups and the considerable morphological at least three (cycads, conifers, Ginkgo) of the fi ve extant divergence among them, as well as the extinction of many lineages of seed plants had probably diverged (Kenrick and lineages. The tremendous morphological gap among ex- Crane 1997; Donoghue and Doyle 2000). In contrast, the tant and fossil seed plant lineages has complicated and ul- angiosperms are relatively young— their earliest unambigu- timately compromised efforts to reconstruct relationships ous fossil evidence is from the Early Cretaceous (~130 mya) with morphology because of homoplasy and uncertainty although molecular dating methods infer older dates for about the homology of structures (e.g., Doyle 1998a, 2006, their origin (see Chapter 2). 2012; Donoghue and Doyle 2000; Soltis et al. 2005b, Relationships among the lineages of extant seed plants, 2008b; Friis et al. 2011). as well as the relationships of living groups to fossil lin- Although progress has been made in elucidating rela- eages, have been issues of longstanding interest and debate. tionships among extant seed plants using DNA sequence A topic of particular intrigue has been the closest relatives data, relationships remain problematic. Even with the ad- of the angiosperms. Angiosperms are responsible either di- dition of more taxa and more genes representing all three rectly or indirectly for the majority of human food and ac- plant genomes, issues remain. Resolution of relationships count for a huge proportion of photosynthesis and carbon among extant seed plants with DNA sequence data has also sequestration. They have diversifi ed to include 350,000– been diffi cult because some lineages have relatively short 400,000 species in perhaps 130– 170 myr and now occur branches (e.g., angiosperms or Pinaceae), whereas other in nearly all habitable terrestrial environments and many clades (e.g., Gnetales) have long branches. This problem is aquatic habitats. Understanding how angiosperms accom- further compounded by the presence in most analyses of plished this is of fundamental evolutionary and ecological long branches to the sister group of seed plants (monilo- importance. phytes). In groups such as the angiosperms and conifers, At some point, nearly every living and fossil group of more taxa can be added to break up long branches, but gymnosperms has been proposed as a possible ancestor of this is not possible across seed plants as a whole given the the angiosperms (e.g., Wieland 1918; Thomas 1934, 1936; considerable extinction that has occurred. Another concern Melville 1962, 1969; Stebbins 1974; Meeuse 1975; Long given the ancient divergences in seed plants is multiple sub- 1977; Doyle 1978, 1998a,b; Retallack and Dilcher 1981; stitutions per site leading to saturation of base substitu- Crane 1985; Cronquist 1988; Crane et al. 1995; reviewed tions. Hence, whereas the use of morphological characters in Doyle 2006, 2008, 2012; Friis et al. 2011). Among ex- has been criticized in seed plant phylogeny (and in a global tant seed plants, the relationship between angiosperms and sense by Scotland et al. 2003), DNA has its own problems Gnetales has received considerable attention. and certainly has not been a consistent solution to resolve Ascertaining the closest relatives of the angiosperms is relationships among extant seed plants (see Burleigh and not only of great systematic importance but also critical Mathews 2004, 2007; Mathews 2009; Mathews et al. for assessing character evolution. For example, the out- 2010; Soltis et al. 2005b, 2008b). come of investigations of character evolution among basal As stressed by other investigators, a complete under- angiosperms, including studies focused on the origin and standing of seed plant phylogeny is not possible with- diversifi cation of crucial angiosperm structures (e.g., fl oral out the integration of fossils. Many investigations have Relationships of Angiosperms 3 attempted this integration (e.g., Crane 1985; Doyle and and “fl ower- like” reproductive organs (Fig. 1.1) (see also Donoghue 1986; Doyle 1996, 1998a,b, 2001, 2006, reviews by Doyle 1996; Frohlich 1999). However, the rea- 2008, 2012; Frohlich 1999; Donoghue
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