Spotlights
Why are there so few species of ferns? Tom A. Ranker1 and Michael A. Sundue1,2 1 2
Department of Botany, University of Hawai’i at Ma¯noa, 3190 Maile Way, Honolulu, HI 96822, USA The Pringle Herbarium, Department of Plant Biology, The University of Vermont, 27 Colchester Ave., Burlington, VT 05405, USA
A recent study has documented a natural hybridization event between two fern lineages that last shared a common ancestor about 60 million years ago. This is one of the deepest hybridization events ever described and has important implications for plant speciation theory. Renowned plant evolutionist G. Ledyard Stebbins published a paper in 1981 entitled ‘Why are there so many species of flowering plants?’ [1], in reference to the fact that of the roughly 285 000 species of land plants, at least 250 000 are angiosperms (as cited by Stebbins). By contrast, only about 10 000 are ferns. The remaining nonflowering lineages combined (hornworts, liverworts, mosses, lycophytes, and gymnosperms) only account for another 23 000. More recent estimates of the number of flowering plants range as high as 450 000 [2], which, if accurate, decreases considerably the proportion of nonflowering land plants. Numerous other studies before and after Stebbins [1] have directly or indirectly addressed Stebbins’ question and have offered a variety of explanations often suggesting adaptive advantages of having flowers and/or seeds, which are undoubtedly part of the reason [3]. In contrast to Stebbins’ approach, we might ask, ‘Why are there so few species of ferns. . .or hornworts, liverworts, and so on?’ Smith [4] proposed that there may be fewer fern species simply because of the relative ease of dispersal via wind-blown spores leading to broad geographic distributions of species and high rates of gene flow between populations, thus inhibiting divergence and speciation. The situation may be the same for all of the other primarily abiotically dispersed non-flowering plants. By contrast, the primary dependence of most angiosperms on animal dispersal for both pollen and seeds (i.e., up to 80% of species for both; [5] and [6], respectively), or just gravity for seeds, results in generally short dispersal distances, which may allow for greater isolation of populations and, ultimately, greater rates of speciation ([3] and references therein). The recent study by Rothfels et al. [7] sheds light on this issue. They provided evidence that the progenitors of the naturally occurring intergeneric hybrid 3Cystocarpium roskamianum Fraser-Jenk. (Cystopteridaceae) represent lineages that have been diverging for approximately Corresponding author: Ranker, T.A. ([email protected]) Keywords: ferns; speciation; deep hybridization; gene flow. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.05.001
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60 million years, although the particular hybridization event that produced the living, but infertile, individual from the French Pyrenees was apparently quite recent. To put this in perspective, consider the divergence dates of other hybridizations between deeply divergent parental lineages: African cichlids, 8.5 Ma (million years); plethodontid salamanders, 12 Ma; grass genera, 14 Ma; tulip tree species, 10–15 Ma; hylid treefrogs, 34 Ma; and sunfish, 37 Ma (see references in [7]). Thus, the lineages of the parental taxa of 3Cystocarpium have been separated by 1.5 times longer than the deepest known hybridization of animals and about four times longer than those of flowering plants. Rothfels et al. [7] amplified and cloned the single-copy nuclear marker gapCp from 3Cystocarpium roskamianum and compared the four alleles discovered to 48 gapCp sequences of other taxa in Cystopteridaceae, including species of the inferred parental genera Cystopteris and Gymnocarpium (i.e., based on the morphologically based hypothesis of Fraser-Jenkins [8]). The results of phylogenetic and sequential empirical Bayesian analyses supported (i) a hybrid origin of 3Cystocarpium involving a cross between the cosmopolitan allotetraploid Gymnocarpium dryopteris (L.) Newman and a European member of the Cystopteris fragilis (L.) Bernhardi complex and (ii) a mean age estimate for the most recent common ancestor of the two parental genera of 57.9 Ma (95% highest posterior density interval spanning 40.2–76.2 Ma). As the authors state (p. 438), this result ‘. . .provides a new upper limit for the length of time it may take before reproductive barriers are complete, in this case, a cumulative total of 120 million years of independent evolution (60 million years for each parent lineage).’ Interestingly, observations of chromosome pairing during meiosis I showed that some homologous chromosomes could still form loose bivalents, although most were present as univalents. Rothfels et al. [7] point out that other natural hybridizations between deeply divergent lineages that may rival the case of 3Cystocarpium are only known from plants that rely on abiotic dispersal factors such as wind and water; i.e., a gymnosperm (Cupressaceae), a Selaginella (Selaginellaceae, a lycophyte), and four other fern hybrids (see references in [7]). In addition, there are intersubgeneric hybrids in the ancient fern genus Osmunda (Osmundaceae) whose parental taxon lineages have been diverging for 100–215 million years (e.g., see [9–11]). Rothfels et al. [7] discuss various possibilities for the relative roles of prezygotic barriers to hybridization and postzygotic hybrid inviability in the evolution of reproductive isolation in groups with abiotically vs. biotically mediated reproduction. As
Spotlights the authors state, however, regardless of the exact mechanisms involved, the slower evolution of reproductive isolation in non-flowering land plants compared to flowering plants may account for the relative paucity of species, in part, by enforcing a ‘low birth rate of new species.’ The relatively high rates of gene flow that would follow from wind-mediated spore dispersal would reduce the rate of formation of any kind of barriers to hybridization. This hypothesis is certainly in line with the idea that gene flow is a potent evolutionary force in plants [12]. Concluding remarks The impressive species richness of the flowering plants is undoubtedly due to many interacting factors that vary in their effects across lineages. By contrast, though, could the lower speciation rates of ferns and other abiotically dispersed, non-flowering land plants primarily be driven by high rates of gene flow? References 1 Stebbins, G.L. (1981) Why are there so many species of flowering plants? Bioscience 31, 573–577 2 Pimm, S.L. and Joppa, L.N. (2015) How many plant species are there, where are they, and at what rate are they going extinct? Ann. Missouri Bot. Gard. 100, 170–176
Trends in Plant Science July 2015, Vol. 20, No. 7
3 Crepet, W.L. and Niklas, K.J. (2009) Darwin’s second ‘‘abominable mystery’’: Why are there so many angiosperm species? Am. J. Bot. 96, 366–381 4 Smith, A.R. (1972) Comparison of fern and flowering plant distributions with some evolutionary interpretations for ferns. Biotropica 4, 4–9 5 Ackerman, J.D. (2000) Abiotic pollen and pollination: ecological, functional, and evolutionary perspectives. Plant Syst. Evol. 222, 167–185 6 Traveset, A. et al. (2014) The ecology of seed dispersal. In Seeds: the ecology of regeneration in plant communities (3rd Edition) (Gallagher, R.S., ed.), pp. 62–93, CAB International 7 Rothfels, C.J. et al. (2015) Natural hybridization between genera that diverged from each other approximately 60 million years ago. Am. Nat. 185, 433–442 8 Fraser-Jenkins, C.R. (2008) Taxonomic revision of three hundred Indian subcontinental pteridophytes with a revised census-list: a new picture of fern-taxonomy and nomenclature in the Indian subcontinent. Bishen Singh Mahendra Pal Singh, Dehra Dun, India 9 Tsutsumi, C. et al. (2011) A new allotetraploid species of Osmunda (Osmundaceae). Syst. Bot. 36, 836–844 10 Schneider, H. et al. (2015) Are the genomes of royal ferns really frozen in time? Evidence for coinciding genome stability and limited evolvability in the royal ferns. New Phytol. http://dx.doi.org/10.1111/ nph.13330 11 Bomfleur, B. et al. (2014) Fossilized nuclei and chromosomes reveal 180 million years of genomic stasis in royal ferns. Science 343, 1376– 1377 12 Ellstrand, N. (2014) Is gene flow the most important evolutionary force in plants? Am J. Bot. 101, 737–753
Active pollinator choice by Heliconia ‘fits the bill’ Judith L. Bronstein and Sarah K. Richman Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721 USA
A new study documents that a tropical plant only reproduces when pollen has been deposited by a visitor capable of extracting nectar from its deep flowers. Large, long-billed hummingbirds generally carry greater quantities of, and more genetically diverse, pollen. Thus, plants can exert more active partner choice than previously considered possible. A hummingbird inserting its long bill into a red, tubular flower is an iconic image of pollination. Although this image leads one to think about trait-matching and pairwise coevolution, as a rule each pollinator species visits more than one plant species, which in turn is visited by more than one pollinator [1]. On each side of the mutualism, some partners confer higher benefits than others. How can plants and animals filter out the worst partners, and consistently associate with the best? Pollinators commonly learn to discriminate among plants, choosing those likely to offer the most nectar [2]. By contrast, plants have been thought incapable of assessing pollinator quality and then acting instantaneously upon this information. RathCorresponding author: Bronstein, J.L. ([email protected]) Keywords: coevolution; hummingbird; partner choice; pollination; reproduction; mutualism. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.04.010
er, researchers have focused on how evolved traits, such as corolla length and nectar chemistry, allow plants to attract and reward the best pollinators. Such mechanisms are far from perfect, though. Plants lose much of their nectar to visitors that deposit low-quality pollen (or none at all). However, a new study by Matthew Betts, Adam Hadley, and John Kress[3] suggests that plants may be more able to selectively associate with good pollinators than has previously been thought possible. Heliconia tortuosa Griggs (Heliconiaceae) possesses long, tubular, curved, yellow flowers which are held within bright red bracts. In Costa Rica, they are visited by a suite of hummingbird species that vary considerably in traits likely to affect their quality as pollinators. Betts et al. started their study of H. tortuosa with a standard experiment in pollination biology: they compared pollentube formation between flowers exposed to hummingbirds in nature, and flowers protected from hummingbirds but pollinated by hand. Perplexingly, flowers given an excess of hand-deposited pollen initiated fewer pollen tubes, not more. This effect, however, disappeared when the researchers also drained the nectar during the handpollination treatment. Betts et al. formulated a clever explanation for these odd results. They conjectured that the plant will only invest in reproduction if some type of 403
Why are there so few species of ferns? Tom A. Ranker1 and Michael A. Sundue1,2 1 2
Department of Botany, University of Hawai’i at Ma¯noa, 3190 Maile Way, Honolulu, HI 96822, USA The Pringle Herbarium, Department of Plant Biology, The University of Vermont, 27 Colchester Ave., Burlington, VT 05405, USA
A recent study has documented a natural hybridization event between two fern lineages that last shared a common ancestor about 60 million years ago. This is one of the deepest hybridization events ever described and has important implications for plant speciation theory. Renowned plant evolutionist G. Ledyard Stebbins published a paper in 1981 entitled ‘Why are there so many species of flowering plants?’ [1], in reference to the fact that of the roughly 285 000 species of land plants, at least 250 000 are angiosperms (as cited by Stebbins). By contrast, only about 10 000 are ferns. The remaining nonflowering lineages combined (hornworts, liverworts, mosses, lycophytes, and gymnosperms) only account for another 23 000. More recent estimates of the number of flowering plants range as high as 450 000 [2], which, if accurate, decreases considerably the proportion of nonflowering land plants. Numerous other studies before and after Stebbins [1] have directly or indirectly addressed Stebbins’ question and have offered a variety of explanations often suggesting adaptive advantages of having flowers and/or seeds, which are undoubtedly part of the reason [3]. In contrast to Stebbins’ approach, we might ask, ‘Why are there so few species of ferns. . .or hornworts, liverworts, and so on?’ Smith [4] proposed that there may be fewer fern species simply because of the relative ease of dispersal via wind-blown spores leading to broad geographic distributions of species and high rates of gene flow between populations, thus inhibiting divergence and speciation. The situation may be the same for all of the other primarily abiotically dispersed non-flowering plants. By contrast, the primary dependence of most angiosperms on animal dispersal for both pollen and seeds (i.e., up to 80% of species for both; [5] and [6], respectively), or just gravity for seeds, results in generally short dispersal distances, which may allow for greater isolation of populations and, ultimately, greater rates of speciation ([3] and references therein). The recent study by Rothfels et al. [7] sheds light on this issue. They provided evidence that the progenitors of the naturally occurring intergeneric hybrid 3Cystocarpium roskamianum Fraser-Jenk. (Cystopteridaceae) represent lineages that have been diverging for approximately Corresponding author: Ranker, T.A. ([email protected]) Keywords: ferns; speciation; deep hybridization; gene flow. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.05.001
402
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60 million years, although the particular hybridization event that produced the living, but infertile, individual from the French Pyrenees was apparently quite recent. To put this in perspective, consider the divergence dates of other hybridizations between deeply divergent parental lineages: African cichlids, 8.5 Ma (million years); plethodontid salamanders, 12 Ma; grass genera, 14 Ma; tulip tree species, 10–15 Ma; hylid treefrogs, 34 Ma; and sunfish, 37 Ma (see references in [7]). Thus, the lineages of the parental taxa of 3Cystocarpium have been separated by 1.5 times longer than the deepest known hybridization of animals and about four times longer than those of flowering plants. Rothfels et al. [7] amplified and cloned the single-copy nuclear marker gapCp from 3Cystocarpium roskamianum and compared the four alleles discovered to 48 gapCp sequences of other taxa in Cystopteridaceae, including species of the inferred parental genera Cystopteris and Gymnocarpium (i.e., based on the morphologically based hypothesis of Fraser-Jenkins [8]). The results of phylogenetic and sequential empirical Bayesian analyses supported (i) a hybrid origin of 3Cystocarpium involving a cross between the cosmopolitan allotetraploid Gymnocarpium dryopteris (L.) Newman and a European member of the Cystopteris fragilis (L.) Bernhardi complex and (ii) a mean age estimate for the most recent common ancestor of the two parental genera of 57.9 Ma (95% highest posterior density interval spanning 40.2–76.2 Ma). As the authors state (p. 438), this result ‘. . .provides a new upper limit for the length of time it may take before reproductive barriers are complete, in this case, a cumulative total of 120 million years of independent evolution (60 million years for each parent lineage).’ Interestingly, observations of chromosome pairing during meiosis I showed that some homologous chromosomes could still form loose bivalents, although most were present as univalents. Rothfels et al. [7] point out that other natural hybridizations between deeply divergent lineages that may rival the case of 3Cystocarpium are only known from plants that rely on abiotic dispersal factors such as wind and water; i.e., a gymnosperm (Cupressaceae), a Selaginella (Selaginellaceae, a lycophyte), and four other fern hybrids (see references in [7]). In addition, there are intersubgeneric hybrids in the ancient fern genus Osmunda (Osmundaceae) whose parental taxon lineages have been diverging for 100–215 million years (e.g., see [9–11]). Rothfels et al. [7] discuss various possibilities for the relative roles of prezygotic barriers to hybridization and postzygotic hybrid inviability in the evolution of reproductive isolation in groups with abiotically vs. biotically mediated reproduction. As
Spotlights the authors state, however, regardless of the exact mechanisms involved, the slower evolution of reproductive isolation in non-flowering land plants compared to flowering plants may account for the relative paucity of species, in part, by enforcing a ‘low birth rate of new species.’ The relatively high rates of gene flow that would follow from wind-mediated spore dispersal would reduce the rate of formation of any kind of barriers to hybridization. This hypothesis is certainly in line with the idea that gene flow is a potent evolutionary force in plants [12]. Concluding remarks The impressive species richness of the flowering plants is undoubtedly due to many interacting factors that vary in their effects across lineages. By contrast, though, could the lower speciation rates of ferns and other abiotically dispersed, non-flowering land plants primarily be driven by high rates of gene flow? References 1 Stebbins, G.L. (1981) Why are there so many species of flowering plants? Bioscience 31, 573–577 2 Pimm, S.L. and Joppa, L.N. (2015) How many plant species are there, where are they, and at what rate are they going extinct? Ann. Missouri Bot. Gard. 100, 170–176
Trends in Plant Science July 2015, Vol. 20, No. 7
3 Crepet, W.L. and Niklas, K.J. (2009) Darwin’s second ‘‘abominable mystery’’: Why are there so many angiosperm species? Am. J. Bot. 96, 366–381 4 Smith, A.R. (1972) Comparison of fern and flowering plant distributions with some evolutionary interpretations for ferns. Biotropica 4, 4–9 5 Ackerman, J.D. (2000) Abiotic pollen and pollination: ecological, functional, and evolutionary perspectives. Plant Syst. Evol. 222, 167–185 6 Traveset, A. et al. (2014) The ecology of seed dispersal. In Seeds: the ecology of regeneration in plant communities (3rd Edition) (Gallagher, R.S., ed.), pp. 62–93, CAB International 7 Rothfels, C.J. et al. (2015) Natural hybridization between genera that diverged from each other approximately 60 million years ago. Am. Nat. 185, 433–442 8 Fraser-Jenkins, C.R. (2008) Taxonomic revision of three hundred Indian subcontinental pteridophytes with a revised census-list: a new picture of fern-taxonomy and nomenclature in the Indian subcontinent. Bishen Singh Mahendra Pal Singh, Dehra Dun, India 9 Tsutsumi, C. et al. (2011) A new allotetraploid species of Osmunda (Osmundaceae). Syst. Bot. 36, 836–844 10 Schneider, H. et al. (2015) Are the genomes of royal ferns really frozen in time? Evidence for coinciding genome stability and limited evolvability in the royal ferns. New Phytol. http://dx.doi.org/10.1111/ nph.13330 11 Bomfleur, B. et al. (2014) Fossilized nuclei and chromosomes reveal 180 million years of genomic stasis in royal ferns. Science 343, 1376– 1377 12 Ellstrand, N. (2014) Is gene flow the most important evolutionary force in plants? Am J. Bot. 101, 737–753
Active pollinator choice by Heliconia ‘fits the bill’ Judith L. Bronstein and Sarah K. Richman Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721 USA
A new study documents that a tropical plant only reproduces when pollen has been deposited by a visitor capable of extracting nectar from its deep flowers. Large, long-billed hummingbirds generally carry greater quantities of, and more genetically diverse, pollen. Thus, plants can exert more active partner choice than previously considered possible. A hummingbird inserting its long bill into a red, tubular flower is an iconic image of pollination. Although this image leads one to think about trait-matching and pairwise coevolution, as a rule each pollinator species visits more than one plant species, which in turn is visited by more than one pollinator [1]. On each side of the mutualism, some partners confer higher benefits than others. How can plants and animals filter out the worst partners, and consistently associate with the best? Pollinators commonly learn to discriminate among plants, choosing those likely to offer the most nectar [2]. By contrast, plants have been thought incapable of assessing pollinator quality and then acting instantaneously upon this information. RathCorresponding author: Bronstein, J.L. ([email protected]) Keywords: coevolution; hummingbird; partner choice; pollination; reproduction; mutualism. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.04.010
er, researchers have focused on how evolved traits, such as corolla length and nectar chemistry, allow plants to attract and reward the best pollinators. Such mechanisms are far from perfect, though. Plants lose much of their nectar to visitors that deposit low-quality pollen (or none at all). However, a new study by Matthew Betts, Adam Hadley, and John Kress[3] suggests that plants may be more able to selectively associate with good pollinators than has previously been thought possible. Heliconia tortuosa Griggs (Heliconiaceae) possesses long, tubular, curved, yellow flowers which are held within bright red bracts. In Costa Rica, they are visited by a suite of hummingbird species that vary considerably in traits likely to affect their quality as pollinators. Betts et al. started their study of H. tortuosa with a standard experiment in pollination biology: they compared pollentube formation between flowers exposed to hummingbirds in nature, and flowers protected from hummingbirds but pollinated by hand. Perplexingly, flowers given an excess of hand-deposited pollen initiated fewer pollen tubes, not more. This effect, however, disappeared when the researchers also drained the nectar during the handpollination treatment. Betts et al. formulated a clever explanation for these odd results. They conjectured that the plant will only invest in reproduction if some type of 403
