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Key Concepts -- Lecture 11 (origin of angiosperms, part 2) IB 168 Spring 2009 Why are there no angiosperm fossils until the Cretaceous? That is, how do we account for 100+ million year gap in the fossil record between the time when angiosperms split from their closest living relatives (sometime in the Paleozoic, probably, based on first fossil occurrences of most modern gymnosperm groups then) and their first appearance in the fossil record? An important distinction needs to be made between the angiosperm stem lineage and the angiosperm crown group in discussing the angiosperm fossil record and origin: Stem group Sp. A Sp. B Sp. C Crown group Stem lineage = The line predating the most recent common ancestor of all modern angiosperms and running back to the most recent common ancestor with at least one of the modern gymnosperm groups (that is, the living sister group) . Members of the stem lineage should have some subset of the diagnostic (derived) characteristics of angiosperms. Crown group: The least-inclusive clade including all modern angiosperms; that is, the group that descended from the most recent common ancestor of all living groups of angiosperms. Possibly, a known fossil (extinct) taxon such as Caytonia (a seed fern) or a member of Bennettitales (cycadioids) may belong to the angiosperm stem lineage but no fossil members of the crown group of angiosperms have been found earlier than the Cretaceous. The great amount of evolutionary change that must have occurred along the angiosperm stem lineage makes difficult any determination of whether a fossil plant belongs to that lineage or not (hard to predict what it would look like). Referring to Doyle & Donoghue 1993 scenarios for angiosperm origins on handout from previous lecture on this topic (that is, the four trees labelled a--d, below the Crane 1987 and Friis et al. 1987 tables) Four scenarios of angiosperm origin (Doyle & Donoghue 1993): All but Tree b suggest that the fossil record of modern angiosperms is flawed (incomplete); leaf & pollen data of Doyle and Hickey from the Potomac Formation suggest otherwise and show a transition from plesiomorphic leaves and pollen to more derived leaf and pollen types in early Cretaceous fossil record (see notes from previous lecture). In all four trees, node "A" represents the most recent common ancestor between angiosperms and their sister group among living gymnosperms; node "B" represents the most recent common ancestor of all modern (living) angiosperms. The stem lineage of angiosperms runs from B to A; the crown group of angiosperms includes all descendants of B. By the time that B arose (but possibly not before that time), all characteristics shared by modern angiosperms would have been in place. The above considerations are critical for understanding the arguments below about the four tree scenarios, Tree a through Tree d. Tree "a" = Upland hypothesis: An idea from the 1960s (Axelrod's) that modern angiosperms (the crown group) arose long before the first fossils appear and underwent extensive diversification then, but they all occurred in well-drained, mountainous situations where likelihood of fossil preservation would be poor. Under this scenario, the fossil record is flawed because the ecological setting of the plants prior to the Cretaceous was not conducive to fossilization (speculative). Tree "b" indicates that modern angiosperms (the crown group) arose when they first appear in the fossil record. This scenario suggests that the fossil record accurately reflects the time of origin of modern angiosperms and that the features shared by modern angiosperms may have been sufficient for their explosive diversification. Tree "c" indicates that the crown group of angiosperms is much older than the Cretaceous but that extensive diversification of angiosperms did not occur until the Cretaceous AND only occurred in one of the angiosperm lineages. This scenario implies that one or more characteristics that arose AFTER all of the shared features of angiosperms were in place was/were critical to explosive diversification of the group; that is, one or more "key innovation(s)" of one of the modern angiosperm lineages -- above and beyond the features shared by all angiosperms -- was necessary for the tremendous burst of diversity that we see in the Cretaceous. Tree "d" is similar to "a" and "c" in indicating that the crown group of angiosperms is much older than the Cretaceous; the difference here is that extensive diversification began in all angiosperm lineages (not just in one of them) in the Cretaceous. This scenario suggests that some environmental change in Cretaceous led to success of the angiosperms; that is, their shared characteristics made them "preadapted" for success, but only after some "key opportunity" arose, associated with the environment, not with a "key innovation" of one of the lineages. Recent success at resolving relationships among early-diverging modern lineages of angiosperms gives an indication of character evolution and ancestral characteristics of angiosperms -- and refinement of the above hypotheses. Recent analyses of molecular data have converged on one basal topology for the angiosperms -- the so-called "ANITA grade." [ANITA is an acronym that includes the first letters of each of the taxa included within it: Amborella, Nymphaeales, Illiciales, Trimenia, Austrobaileya] Amborella (1) Nymphaeales (85) "ANITA" Illiciales (90) grade Trimeniaceae (5) Austrobaileya (1) Magnoliids (>10,000) Monocots (>55,000) "Eudicots" (>190,000) The first evidence of the ANITA grade was from a phylogenetic analysis of phytochrome genes -- Mathews & Donoghue's study, published in Science in 1999 (see handout), overcame possible long-branch attraction between outgroup and ingroup lineages that might have led to an inaccurate rooting of the tree. By sequencing both copies of the gene, which evidently underwent a duplication (yielding genes PHY A and PHY C) just prior to the origin of modern angiosperms, they were able to root the angiosperm phylogeny without an outgroup, by placing the root between the two gene trees. Less than a month later, Qiu et al. published a paper in Nature based on phylogenetic analysis of 5 genes (from all 3 plant genomes) analysis. They used many more taxa than Mathews and Donoghue and included gymnosperms -- to root the tree using an outgroup -- and came up with basically the same result: the ANITA grade was basal in the angiosperm tree. Implications of ANITA grade for ancestral features of modern angiosperms (many of the features were suggested earlier to be primitive in angiosperms, by the early 20th- Century botanist Bessey, for example) The features below are shared by some or all of the different lineages of the ANITA grade and are therefore suggested to have been features found in the most recent common ancestor of all living angiosperms: - Two cotyledons (dicots, not monocots) - Uniaperturate pollen (not triaperturate) - Carpels sealed by secretions (not fused); ascidiate (barrel-shaped) - Lack of differentiation of sepals and petals (tepals) - Indeterminate (variable) numbers of tepals, stamens, and carpels - Spiral arrangement of floral parts - Lack of fusion of floral parts - Self-incompatibility = pollen cannot fertilize ovules from the same plant - No vessels (but other vessel-less angiosperms (e.g., Winteraceae) evidently represent a loss of vessels) - Occurrence in sporadically disturbed sites in shady forest understories ("Dark and Disturbed" ecology). Diversification rate accelerated well after the origin of angiosperms Lineages of the ANITA grade are low in diversity (Amborella 1 sp., Austrobaileya 1 sp., Trimenia 2-5 spp., Nymphaeales 70-80 spp, Illiciales (80 spp.). By comparison, the diversity of lineages above the ANITA grade is tremendous (>100× as diverse); therefore, some change that occurred in the lineage above the ANITA grade may have been critical to angiosperm success. Earliest Cretaceous angiosperm fossils show features of ANITA grade not seen in most other living angiosperms (e.g., barrel-shaped carpel morphology). Based on the evidence that the earliest Cretaceous fossils were like ANITA grade members and that a high rate of diversification of angiosperms appears to have occurred not at the base of the angiosperm tree, but instead after divergence of the ANITA lineages, the scenario for origin of angiosperms may combine elements of Tree b & Tree c models (from previous page); that is, as in Tree b, the angiosperm fossil record may be fairly accurate about the time of origin of the crown group of angiosperms, but some characteristic(s) ("key innovation") of a subset of the modern angiosperm lineages may have been critical to their explosive diversification (as in Tree c). .
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