Detailed Seed Cone Morpho-Anatomy Provides New Insights into Seed Cone Origin and Evolution of Podocarpaceae; Podocarpoid and Dacrydioid Clades
Abstract
:1. Introduction
2. Material and Methods
2.1. Seed Cone Collection
2.2. Morphology and Distribution of the Investigated Taxa
- The South African Afrocarpus falcatus (Thunb.) C.N. Page, which forms large trees [21].
- Two species of Nageia, N. nagi (Thunb.) Kuntze, which is an evergreen tall tree, distributed in China (introduced), Japan, Taiwan (introduced) and Vietnam [21,22] and N. wallichiana (Presl.) Kuntze, which is a tall tree distributed in Brunei Darussalam, Cambodia, China, India, Indonesia, Laos, Malaysia, Myanmar, Papua New Guinea, the Philippines, Thailand and Vietnam [21,22]).
- Three species of Podocarpus subgenus Podocarpus (P. henkelii Stapf., P. elongatus (Aiton) L’Herit. Ex Persoon and P. oleifolius D. Don). Podocarpus henkelii and P. elongatus occur in southern Africa, while P. oleifolius is found in Central America [23].
- Two species of Podocarpus subgenus Foliolatus (P. spinulosus (Smith) R. Br. Ex Mirbel and P. elatus R. Br. ex Endlicher). Podocarpus spinulosus and P. elatus are dioecious species from northeastern Australia [24].
- Retrophyllum comptonii (Buchholz) C.N. Page, which is a tree endemic to New Caledonia [25].
- Dacrycarpus dacrydioides (A. Richard.) de Laub., a tall tree endemic to New Zealand.
- Dacrydium cupressinum Solander ex G. Forst., a tall tree endemic to New Zealand.
- Falcatifolium papuanum de Laub., a tall tree endemic to Papua New Guinea [26].
2.3. Taxon Processing and Sectioning
2.4. Measurements and Trait Reconstructions
3. Results
3.1. Afrocarpus Seed Cone Morpho-Anatomy
3.2. Nageia Seed Cone Morpho-Anatomy
3.3. Podocarpus Seed Cone Morpho-Anatomy
3.3.1. Podocarpus henkelii
3.3.2. Podocarpus elongatus
3.3.3. Podocarpus oleifolius
3.3.4. Podocarpus spinulosus
3.3.5. Podocarpus elatus
3.4. Retrophyllum Seed Cone Morpho-Anatomy
3.5. Acmopyle Seed Cone Morpho-Anatomy
3.6. Dacrycarpus Seed Cone Morpho-Anatomy
3.7. Dacrydium Seed Cone Morpho-Anatomy
3.8. Falcatifolium Seed Cone Morpho-Anatomy
3.9. Comparison of Seed Cone Morpho-Anatomical Characters
3.10. Seed Cone Morpho-Anatomical Traits and Structures
3.10.1. Fleshy Seed Cones
3.10.2. Epimatium Morphology
3.10.3. Receptaculum Morphology
3.10.4. Testa Morpho-Anatomy
3.10.5. Ovule and Embryo Traits
4. Discussion
4.1. The Dominance of Fleshy Seed Cones in Living Podocarps and Fossil Evidence
4.2. Shifts in the Fleshy Structures
4.3. Significance of the Evolutionary Reconstruction of Fleshiness
4.4. Broader Perspective with other Podocarps
4.5. Evolution of Morphological Structures and Animal Dispersal
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
References
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Characters | Afrocarpus falcatus | Nageia wallichiana | Nageia nagi | Podocarpus henkelii (subgenus Podocarpus) | Podocarpus elongatus (subgenus Podocarpus) | Podocarpus oleifolius (subgenus Podocarpus) | Podocarpus spinulosus (subgenus Foliolatus) | Podocarpus elatus (subgenus Foliolatus) | Retrophyllum comptonii | Dacrydium cupressinum | Dacrycarpus dacrydioides | Falcatifolium papuanum | Acmopyle pancheri |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Reproductive cycle | 1 year | 1 year | 1 year | 1 year | 1 year | 1 year | 1 year | 1 year | 1 year | 2 years | 1 year | 1 year | 1–2 years |
Cone shape | obovoid | ovoid | globose | obovoid | ovoid | ovoid | ovoid | ovoid | ovoid-subglobose | obovoid | ovoid | obovoid | ovoid |
Cone size (mm) | 12–20 × 8–16 | 18–38 × 6–10 | 12–18 × 10–16 | 15–20 × 8–12 | 13–20 × 4–8 | 12–22 × 4–7 | 11–24 × 6–7 | 25–45 × 10–20 | 10–20 × 7–15 | 6–10 × 2–4 | 10–18 × 4–8 | 10–16 × 4–6 | 18–34 × 10–18 |
Colour | yellowish | reddish | brown | yellowish | reddish | reddish | dark purple | dark purple | reddish | reddish | reddish | reddish | reddish-brown |
Number of seeds per cone | 1 | 1–2 | 1 | 1 | 1 | 1–2 | 1 | 1–2 | 1–2 | 1 | 1–2 | 1 | 1–2 |
Seed size (mm) | 8–18 × 6–14 | 14–20 × 10–16 | 10–15 × 8–12 | 12–17 × 4–6 | 6–12 × 3–5 | 5–8 × 3–6 | 8–10 × 5–7 | 15–20 × 12–15 | 7–17 × 5–12 | 2.5–6 × 2–3 | 6–10 × 4–8 | 6–7 × 4–5 | 6–8 × 5–7 |
Seed surface | rugose | rugose | rugose | rugose | smooth | smooth | rugose | rugose | rugose | smooth | smooth | smooth | rugose |
Seed colour | brown | brown | brown | light brown | brown | brown | brown | purplish black | brown | brownish black | purplish black | dark brown | brown |
Ovule orientation | inverted | inverted | inverted | inverted | inverted | inverted | inverted | inverted | inverted | inverted | inverted | inverted | erect |
Cuticle | thick | thick | thick | thick | thin | thin | thin | thin | thick | thick | thin | thin | thick |
Epidermal layers | 1 | 1–2 | 1–2 | 1 | 1 | 1 | 1–2 | 1 | 1 | 1 | 1 | 1 | 1 |
Epidermal cell shape | rectangular | round–triangular | round–triangular | round–triangular | round–triangular | rectangular | round–triangular | round–triangular | isodiametric | dome-shaped | dome-shaped | dome-shaped | triangular |
Exotesta | fleshy | coriaceous | coriaceous | fleshy | coriaceous | coriaceous | coriaceous | coriaceous | fleshy | coriaceous | coriaceous | coriaceous | coriaceous |
Exotesta layers of cells | 10–18 | 14–22 | 12–20 | 12–18 | 8–13 | 10–14 | 12–16 | 18–26 | 16–20 | 1–2 | 10–14 | 3–6 | 14–20 |
Mesotesta layers of cells | 3–5 | – | – | 16–22 | 3–5 | 10–16 | – | – | 6–8 | – | – | – | 6–12 |
Endotesta layers of cells | 20–32 | 12–20 | 10–18 | 12–20 | 6–12 | 10–16 | 5–8 | 4–6 | 12–18 | 8–10 | 4–6 | 6–14 | 12–18 |
Nucellus layers | 4–10 | 5–10 | 6–12 | 6–12 | 8–14 | 7–10 | 6–8 | 2–4 | 4–8 | 6–10 | 3–6 | 4–8 | 4–8 |
Embryo (megagametophyte) shape | straight | straight | straight | straight | straight | straight | straight | straight | straight | straight | straight | straight | straight |
Embryo size (mm) | 0.8–1.2 × 0.3–0.5 | 0.8–1.7 × 0.3–0.5 | 0.8–1.5 × 0.3–0.4 | 0.65–1.2 × 0.2–0.4 | 0.5–0.9 × 0.2–0.3 | 0.6–0.8 × 0.2–0.3 | 0.5–1.3 × 0.3–0.5 | 0.7–1.2 × 0.3–0.5 | 0.4–0.9 × 0.2–0.4 | 0.25–0.6 × 0.1–0.2 | 0.6–1.0 × 0.2–0.5 | 0.3–0.6 × 0.15–0.25 | 0.3–6 × 0.1–0.2 |
Bracts | 1–2 | 4–7 | 4–6 | 1–2 | 2 | 2 | 2–4 | 2 | 3–5 | 8–14 | 2–3 | 6–12 | 4–10 |
Stomata on bracts | present | present | present | present | present | present | present | present | present | present | present | present | present |
Epimatium | present | present | present | present | present | present | present | present | present | present | present | present | present |
Epimatium shape | fleshy and fused with outer testa surrounding the whole seed | papery and fused with outer testa surrounding the whole seed | fleshy and fused with outer testa surrounding the whole seed | fleshy and fused with outer testa surrounding the whole seed | papery and fused with outer testa surrounding the whole seed | papery and fused with outer testa surrounding the whole seed | papery and fused with outer testa surrounding the whole seed | papery and fused with outer testa surrounding the whole seed | fleshy and fused with outer testa surrounding the whole seed | fleshy asymmetrical cup-like | papery and fused with outer testa surrounding the whole seed | fleshy asymmetrical cup-like | papery and fused with outer testa surrounding the whole seed |
Epimatium structure | fleshy | fleshy | fleshy | fleshy | papery | papery | papery | papery | fleshy | fleshy | papery | fleshy | papery |
Epimatium colour | yellowish | purple | purple | yellowish | purple | olive green | dark purple | purplish black | reddish | brownish black | purplish black | reddish brown | brown |
Receptaculum | absent | present | absent | absent | present | present | present | present | absent | present | present | present | present |
Receptaculum colour | - | reddish | - | absent | bright red | yellowish red | blueish black | blueish black | - | reddish | orange–red | reddish | reddish brown |
Sclereids | present | present | present | present | present | present | present | present | present | present | present | present | present |
Resin canals | present | present | present | present | present | present | present | present | present | present | present | present | present |
Dispersal | zoochory [birds, bats (Rousettus aegyptiacus), monkeys (Chlorocebus pygerythrus), woodland dormouse (Graphiurus murinus) and Verreaux’s mouse (Myomyscus verreauxii)] | zoochory | zoochory | zoochory (birds) | zoochory (birds) | zoochory (birds) | zoochory (birds) | zoochory (birds) | zoochory | zoochory [New Zealand bellbird (Anthornis melanura) and Tūī (Prosthemadera novaeseelandiae), Kākāpō (Strigops habroptilus)] | zoochory [New Zealand pigeon (Hemiphaga novaeseelandiae), Tūī (Prosthemadera novaeseelandiae) and New Zealand bellbird (Anthornis melanura), Anthornis melanura, Hemiphaga novaeseelandiae, Prosthemadera novaeseelandiae] | zoochory (birds) | zoochory (birds) |
Taxon | Number of Prosuspensor Cells | Number of Binucleate Embryonic Cells | Reference |
---|---|---|---|
Podocarpoid Clade | |||
Afrocarpus | 18–23 | 9–11 | Buchholz, 1941 [30] |
Nageia | 18–23 | 7, 9–11 | # |
Podocarpus glomeratus | 11–13 | 2–3 | # |
P. chinensis | 14–15 | 1–2 | # |
P. lawrencei | 7–10 | 1–2 | # |
P. nivalis | 7–10 | 1–2 | # |
P. totara | 7–10 | 1–2 | # |
P. laetus | 7–10 | 1–2 | # |
P. urbanii | 11–13 | 2–3 | # |
Dacrydioid Clade | |||
Dacrycarpus dacrydioides | 11–14 | 4 or 5 | Buchholz, 1941 [30] |
Dacrydium | 7–11 | 5–9 | # |
Other Podocarpaceae | |||
Phyllocladus | 4–6 | 9–12 | Doyle and Looby, 1939 [31] |
Saxegothaea | 3–4 | 10–12 | # |
Pectinopitys ferruginea | 7–9 | 7–9 | Buchholz, 1941 [30] |
Prumnopitys taxifolia | 6–9 | 9–12 | # |
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Khan, R.; Hill, R.S.; Dörken, V.M.; Biffin, E. Detailed Seed Cone Morpho-Anatomy Provides New Insights into Seed Cone Origin and Evolution of Podocarpaceae; Podocarpoid and Dacrydioid Clades. Plants 2023, 12, 3903. https://doi.org/10.3390/plants12223903
Khan R, Hill RS, Dörken VM, Biffin E. Detailed Seed Cone Morpho-Anatomy Provides New Insights into Seed Cone Origin and Evolution of Podocarpaceae; Podocarpoid and Dacrydioid Clades. Plants. 2023; 12(22):3903. https://doi.org/10.3390/plants12223903
Chicago/Turabian StyleKhan, Raees, Robert S. Hill, Veit M. Dörken, and Ed Biffin. 2023. "Detailed Seed Cone Morpho-Anatomy Provides New Insights into Seed Cone Origin and Evolution of Podocarpaceae; Podocarpoid and Dacrydioid Clades" Plants 12, no. 22: 3903. https://doi.org/10.3390/plants12223903