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Los Origenes de Las Plantas Con Flores y Polinizadores
Los Origenes de Las Plantas Con Flores y Polinizadores
EVOLUTION
PHOTO: JONATHAN BLAIR/NATIONAL GEOGRAPHIC IMAGE COLLECTION
By Casper J. van der Kooi1 and Jeff Ollerton2 tery,” and debates continue about the origin can be dated to the Early Cretaceous (~135
and processes driving angiosperm speciation. million years ago), which has led paleobot-
F
or more than a century there has been a Dating the origin of angiosperms was tradi- anists to reason that they originated during
fascination with the surprisingly rapid tionally the prerogative of paleobotanists that era. It is now increasingly recognized
rise and early diversity of flowering who read the fossil record of plants, but with that angiosperms are probably older than the
plants (angiosperms). Darwin described DNA sequencing becoming increasingly so- oldest fossils, but how much older remains
the seemingly explosive diversification phisticated, molecular dating methods have controversial. When angiosperms originated
of angiosperms as an “abominable mys- come to the table. Many angiosperm fossils is key to understanding the origin and evolu-
Published by AAAS
The aquatic angiosperm Archaefructus of mutation rates across taxa and time.
liaoningensis is one of the earliest fossil Variation in divergence times—which inevi-
angiosperms to have been identified so far. tably occurs in datasets with many species—
frequently leads to overestimation of age (5,
the Late Triassic, >200 million years ago. This 6). Indeed, molecular analyses often push
is ~70 million years (roughly the equivalent of origin dates back in time, including the older
the Jurassic) before the earliest accepted an- lineages, but whether this is a methodologi-
giosperm fossils. This study further suggests cal error remains unclear.
that major radiations (species diversifica- One of the hallmarks of angiosperms is
tion) occurred in the Late Jurassic and Early their relationship with animal pollinators,
Cretaceous, ~165 to 100 million years ago. especially insects. As with plants, the di-
By contrast, an overview of paleobotanical versification of insects is a field with many
evidence (2) refutes a substantive pre-Creta- uncertainties. The origin of several impor-
ceous diversification, with only some specific tant orders of flower-visiting insects (e.g.,
clades (such as water lilies) perhaps originat- Coleoptera, Diptera, Hymenoptera, and
ing during the Late Jurassic. The sequential Lepidoptera) lies in the Permian or Triassic
appearance of different types of fossils and (300 to 200 million years ago) with marked
morphological characteristics is proposed to periods of diversification in the Cretaceous,
render major earlier diversification events which is frequently mentioned to coincide
unlikely, supporting previous studies (3, 4). with the main angiosperm radiation (7).
Although the idea that angiosperms arose However, the timing of the origin of flow-
High diversifcation
Molecular analyses
Coleoptera Diptera
SILURIAN NEOGENE
CAMBRIAN ORDOVICIAN DEVONIAN CARBONIFEROUS PERMIAN TRIASSIC JURASSIC CRETACEOUS PALEOGENE
500 400 300 200 100 Now
Millions of years ago
the scheme of angiosperm evolution, because sects, perhaps flower features have shaped and olfactory traits to long-extinct clades of
even if they occurred at this earlier period, an- trait evolution in these large insect groups. plants that once dominated terrestrial floras.
giosperms were not a dominant plant group There are clear examples of coevolution of Future paleontological discoveries will
in the Jurassic. By contrast, Bennettitales specific floral and pollinator morphological undoubtedly reveal additional fossils, and
and other early seed plants were ecologically characteristics in some systems, such as flo- the use of complementary sequencing ap-
dominant in Late Triassic to Jurassic floras, ral tube length and pollinator tongue length proaches and more sophisticated evolution-
indicating that the transition to insect polli- (12). What about floral features such as color ary models will help to mitigate the limita-
nation in angiosperms arose through these and scent? For example, perhaps floral color tions imposed by the rampant polyploidy
gymnosperm groups. These possibilities are and scent evolved to match pollinator vision in plants that frequently hinders analysis of
more complex than the standard scenarios and olfaction, or vice versa. Alternatively, nuclear genes. Whether Darwin’s question
that envisioned a progression from primitive signal production may have evolved synchro- about the timing of flowering-plant evolution
wind pollination to advanced insect pollina- nously with detection. The basic principles of and radiation will ever be answered remains
tion. They hint at a richer ecological milieu color vision in insects, such as the possession a mystery, but clearly this question and its
of more complex interactions between spe- of three types of photoreceptors (ultraviolet, ecological implications for understanding in-
cies than had previously been appreciated, blue, green), seem to predate flowers regard- sect pollination are complicated. j
including insect groups that are currently less of whether they arose during the Triassic
RE FERENCES AND NOTES
much less important as pollinators, such as or later (13). Because color vision is also used
1. H.-T. Li et al., Nat. Plants 5, 461 (2019).
scorpionflies (Mecoptera) (11). for key behaviors such as detecting potential 2. M. Coiro, J. A. Doyle, J. Hilton, New Phytol. 223, 83 (2019).
The timing of flowering-plant origins mates and predators and finding oviposition 3. S. Magallón, S. Gómez-Acevedo, L. L. Sánchez-Reyes, T.
Hernández-Hernández, New Phytol. 207, 437 (2015).
also provides a minimum age for the evolu- (egg-laying) sites, the evolution of color vi- 4. P. S. Herendeen, E. M. Friis, K. R. Pedersen, P. R. Crane,
tion of their most prominent feature: flow- sion is unlikely to be driven by flower colors. Nat. Plants 3, 17015 (2017).
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Syst. Biol. 64, 869 (2015).
nosperms (e.g., cycads, Ephedra, Gnetum) pared to scent production was documented 6. J. Barba-Montoya et al., New Phytol. 218, 819 (2018).
is facilitated mainly by scent rather than in a group of plants pollinated by scarab bee- 7. S. Cardinal, B. N. Danforth, Proc. R. Soc. B 280,
GRAPHIC: ADAPTED BY N. CARY/SCIENCE FROM E. ZINKSTOK
20122686 (2013).
by visual attraction. The same may have tles (14), where odor reception by pollinators 8. T. J. B. van Eldijk et al., Sci. Adv. 4, e1701568 (2018).
been true of the extinct gymnosperms, but predates production of the scent signal by 9. A. Y. Kawahara et al., Proc. Natl. Acad. Sci. U.S.A. 116,
because scent does not fossilize, it may be plants. However, behavioral aspects of ol- 22657 (2019).
10. J. Ollerton, Annu. Rev. Ecol. Evol. Syst. 48, 353 (2017).
impossible to ever know. However, if the re- faction or color vision, such as innate color 11. D. Ren et al., Science 326, 840 (2009).
productive structures of these extinct gym- preferences that shape foraging behavior in 12. B. Anderson, S. D. Johnson, Evolution 62, 220 (2008).
13. L. Chittka, Isr. J. Plant Sci. 45, 115 (1997).
nosperms functioned in a manner similar various insect groups (15), may have evolved 14. F. P. Schiestl, S. Dötterl, Evolution 66, 2042 (2012).
to their living relatives, with odor predom- later, in response to floral signals. All of this 15. C. J. van der Kooi, A. G. Dyer, P. G. Kevan, K. Lunau, Ann.
inating, then the increasing importance of depends on the timing of the evolution of Bot. 123, 263 (2019).
visual-based cues to attract pollinators in flowering plants as well as the order of evolu- ACKNOWLEDGME NTS
angiosperms could be one of the defining tionary events that led to insect pollination. C.J.v.d.K. is funded by a Veni grant from the Dutch NWO (016.
features of angiosperm evolution and suc- If insect-pollinated gymnosperms predate Veni.181.025) and AFOSR/EOARD (FA9550-15-1-0068). We
cess. Further, if floral structures predate angiosperms, for example, then it may be thank E. Zinkstok for help with the figure.
some speciose orders of flower-visiting in- possible to trace the origin of these visual 10.1126/science.aay3662
Published by AAAS
The origins of flowering plants and pollinators
Casper J. van der Kooi and Jeff Ollerton
REFERENCES This article cites 15 articles, 3 of which you can access for free
http://science.sciencemag.org/content/368/6497/1306#BIBL
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