Biophysical constraints on the origin of leaves inferred from the fossil record

Abstract

The molecular tool kit for producing flat-bladed photosynthetic structures evolved in marine and terrestrial plants during the middle Paleozoic, but it took a further 20 million years before leaves suddenly spread throughout land floras. This delay has long been difficult to explain, given the apparent advantage of leaves for photosynthetic primary production. Theory and experiments predict that exceptionally high atmospheric CO2 levels in the middle Paleozoic delayed the origin of leaves by restricting stomatal development. This would have limited evaporative cooling, leading to lethal overheating of leaves absorbing large quantities of solar energy. Here we test the central prediction of this argument with a morphometric analysis of 300 plant fossils from major European collections. We show a 25-fold enlargement of leaf blades in two phylogenetically independent clades as atmospheric CO2 levels fell during the late Paleozoic. Furthermore, preliminary data suggest that the first abrupt increase in leaf size was accompanied by an 8-fold rise in stomatal density. These evolutionary patterns support the relaxation of biophysical constraints on leaf area predicted by theory and point to a significant role for CO2 in plant evolution.

Fig. 1.

Leaf and atmospheric evolution in the Devonian and Mississippian. (A) Modeled (-○-) (11) or paleosol (•) [CO₂], with a piecewise linear fit (solid line) and error bars indicating range of uncertainty (11). (B) Tropical air temperatures, calculated by assuming radiative forcing by CO₂ (25) above a baseline value of 30°C. (C) Geologic evidence for continental glaciation (solid bars) (11, 19). (D) Maximum leaf or branch width. Range of uncertainty in the age of leaves classified only as Mississippian (Tou-Vis) (gray points and horizontal lines) and maximum size for 10-million-year intervals (solid line). Modeled leaf size with an increasing stomatal density, normalized as a percentage of its maximum value in the Visean (dashed line) and with stomatal density fixed at the mean Early Devonian value (dotted line). (E) Square root of leaf area, with symbols and lines as in D. Stratigraphic abbreviations follow the standard usage and geologic time scale of ref. .

Fig. 2.

Examples of significant Devonian and Mississippian leaf fossils. (A) A. macilenta (Progymnospermopsida, Heist-op-den-Berg, Belgium; Royal Belgian Institute of Natural Sciences, Brussels, catalogue no. 99.730). (B) A. obtusa (Progymnospermopsida, Youngsville, NY; Senckenberg Institute, Frankfurt, catalogue no. SM B16765). (C) Fryopsis frondosa (Lagenostomopsida, Niederburbach, Germany; Natural History Museum, London, catalogue no. V52540). [Bars = 10 mm (A) and 15 mm (B and C).]