Lecture 7: Key Evolutionary Innovations - Leaves and Size

Definition of Key Evolutionary Innovation (KEI): A newly evolved feature that pre-adapts the clade possessing it for new ecological opportunities.
Central Theme: Lecture 7 focuses on leaves and size as critical innovations during the Devonian Period.
Key Discussion Points: * Origination of plant groups in the Devonian. * Structural methods of leaf formation. * The 40-million-year ( $40\,Ma$ ) delay in leaf evolution. * Diverse biological strategies for building trees.

Geologic Timeline: Most major plant groups emerged or had ancestors in the Devonian (referencing Johnson and Troll, 2007).
Major Evolutionary Changes: * Plant Groups: First appearance of ferns and seed plants. All major groups except angiosperms originated or found their ancestors in this period. * Organ Differentiation: The first true leaves, stems, and roots appeared. * Architectural Shifts: Branching patterns and stem structures evolved significantly. * First Forests: The Devonian saw the emergence of the first trees and established forests. * Reproductive Innovations: Transition from homospory to heterospory; evolution of (pre)pollen and seeds.
Origin Patterns: Some innovations had a single origin, while others evolved independently multiple times.

Timeframe: We are observing the results of approximately $470\,Ma$ of evolution (Gensel, 2008).
Non-Vascular Spore Plants (Extant Bryophytes): * Taxa: Liverworts, Hornworts, and Mosses. * Traits: No vascular tissue, possess rhizoids, thin tissues, thin cuticles. * Reproduction: Spores without thin areas in the wall; gametophyte is the dominant generation.
Vascular Spore Plants: * Taxa: Horsetails, Lycopods, and Ferns. * Traits: Vascular tissue, roots, leaves, cuticles with stomata. * Reproduction: Spores with thin areas in the wall; sporophyte is the dominant generation.
Origins of Specific Traits: * Single Origin Innovations: 1. Stomata. 2. Branching in the sporophyte. 3. Specialization of xylem conducting cells (tracheids). 4. Continuous growth. 5. Enclosure of the embryo in a seed. 6. Secondary xylem (wood) in lignophytes. * Independent Evolution (Multiple Origins): 1. Leaves (evolved separately in Lycophytes and Euphyllophytes). 2. Roots (evolved separately in Lycophytes and Euphyllophytes).

The Dichotomy: This split dates back $415\,Ma$ to the Late Silurian-Early Devonian.
Microphylls: * Characteristics: Small size, single vein, no petiole (stalk). * Lineage: Lycophytes (e.g., Selaginella, Lycopodium [Club moss], Isoetes [Quillwort], Spike moss). * Branching: Only occurs at the shoot tip.
Megaphylls: * Characteristics: Large size, complex branched venation, presence of a petiole. * Lineage: Euphyllophytes (includes horsetails, ferns, seed plants, and flowering plants). * Branching: Not limited to the shoot tip.

Enation Theory (for Microphylls): Proposed by Bower (1935) and Steward & Rothwell (1993). * Process: Leaves evolved from simple outgrowths (enations). * Developmental Complexity Lineage: 1. Zosterophyllum: Simple stem. 2. Sawdonia: Emergence of enations. 3. Asteroxylon: Enations receive vascular supply but do not penetrate the leaf fully. 4. Baragwanathia: Fully vascularized microphylls.
Telome Theory (for Megaphylls): Proposed by Steward & Rothwell (1993). * Definition of Telome: One of the branches on a dichotomized axis. * Process: Megaphylls are derived from modified, reduced, and webbed branch systems. * Sequential Stages: 1. Three-dimensional branching (e.g., in early land plants). 2. Planation (flattening of branches into a single plane). 3. Webbing (development of photosynthetic tissue between branches). 4. Further webbing (leading to entire leaves).

Monilophytes (Ferns and Horsetails): * Pertica: The largest known trimerophyte, approximately $1.5\,m$ high. One of the tallest Early Devonian plants; lacked true leaves. * Rhacophyton: Roughly $1.5\,m$ high with secondary growth. It featured 3D-arranged leaf-like branching systems attached to the stem. * Zygopteris illinoiensis: A true fern with flattened leaves subdivided four times.
Lignophytes (Woody Plants): * Archaeopteris halliana: An Upper Devonian "progymnosperm." It was a real tree with a woody stem. * Callixylon: The name for the fossilized wood of Archaeopteris. Its anatomy (radial, tangential, and cross-sections) is remarkably similar to modern conifer wood. * Attributes: Leafy twigs, long-lived roots, and branches that grew synchronously with the trunk.

The Paradox: Evidence suggests the developmental molecular genetics required for leaves were recruited long before large megaphylls became common.
Atmospheric Control: The delay was likely dictated by atmospheric $CO_2$ levels (Beerling, 2005).
Stomata and Thermoregulation: * Stomata regulate $CO_2$ uptake and $H_2O$ transpiration. * They act similarly to sweat glands, preventing leaf overheating.
Early Devonian Conditions: High atmospheric $pCO_2$ levels lead to low stomatal density. In high light and temperature, large leaves would overheat because they could not transpire enough water to cool down.
Late Devonian Transition: As $CO_2$ levels dropped significantly, plants evolved higher stomatal densities. This increased cooling capacity allowed for the evolution of larger, broader megaphylls.
Data Correlation: Observations of fossil megaphyll width show a sharp increase as modeled atmospheric $CO_2$ levels fell (Royer, 2014; Beerling, 2005).

The Gilboa Tree (Cladoxylopsid): * Relative of ferns/horsetails. * Strategy: No leaves, limited root system, and a single long-lived vertical trunk.
Arborescent Lycopsids ("Bark Trees"): * Example: Lepidodendron. * Structure: Thick bark (cortex) provided structural support; relatively small amount of wood (xylem) in the center.
Woody Trees (Lignophytes/Other Trees): * Structure: Support is provided by a thick core of wood (xylem) produced by a cambium; the bark (cortex) is relatively thin compared to the lycopsids.
Timeline of Arborescence: * First trees appeared by Middle Devonian ( $\sim 380\,Ma$ ). * Early forests were dominated by four spore-producing groups and two seed-producing groups. * Lycophytes: Transitioned from small tree-like forms in the Middle Devonian to real trees in the Late Devonian, reaching peak dominance in the Carboniferous.

Vascular System Complexity: Provided increased stability and height.
Secondary Growth: Allowed for a considerable increase in thickness, height, and the effective dispersal of spores.
Environmental Feedback: The combination of tree habits and decreasing $CO_2$ concentrations facilitated the evolution of leaves, resulting in an enormous increase in photosynthetic surface area.