by Piter Kehoma Boll
The theory of sexual selection, based on the idea that there are conflict of interests between males and females, is quite recognized, but almost entirely focused on animals, especially dioecious animals, i.e., animals in which males and females correspond to separate individuals. Meanwhile, hermaphroditic animals and other organisms, such as plants, are usually ignored, but does hermaphroditism or “non-animalism” prevent the occurrence of sexual selection?
The peacock is one of the most famous examples of how sexual selection can drive the evolution of dioecious species. Photo by Oliver Pohlmann.
In the last decades, hermaphroditic animals started to be investigated more deeply concerning sexual conflict as a considerable evolutionary force in these organisms. For example, some studies demonstrated that many hermaphrodites, during copulation, fight to play the role of male, or female, in something called “gender conflict” (which DOES NOT HAVE ANYTHING TO DO with any social aspect of the word “gender”. Here it refers to the sexual role that a hermaphroditic organisms plays during sex).
In plants, on the other hand, the subject is much less explored, especially due to the lack of direct interaction between the two mating organisms. Reproductive strategies in plants were seen, for a long time, as a mean to ensure the supposedly difficult task to unite male and female gametes when one is a sessile organism, i.e., an organism unable to move. After all, this disadvantage forces these organisms to develop special techniques that guarantee the transport of gametes through the environment. With such a relevant problem to assure that sex will happen, it seems absurd to think that plants could yet afford to choose with whom to get laid.
Plants need external agents, such as wind, water or animals, to carry their gametes. Photo by psyberartist (flickr.com/people/10175246@N08).*
So far, the most approached point about sexual selection in plants is related to mechanisms developed by the female part to avoid the ovule to be fertilized by pollen of the same individual (the so-called self-fertilization) or of incompatible individuals (such as pollen of another species or of a close relative, because yes, incest can be a taboo even for plants). Another studied mechanism is related to the prevention of future attempts of fertilization once the zygot has been formed, as an already fertilized flower is not interested in receiving more and more pollen grains.
The passive travel of pollen from the male part to the female one gives us the impression that the male part cannot carry out any intersexual selection. After all, once the pollen arrives at a flower, it cannot leave, so its only chance is to try fertilization in any case, even if it is on an incompatible organism. This also highlights the fact that competition between pollen grains may occur on the female part, on a real race to see who gets first to the ovule. This competition may be controlled by the female part by changings in pollen receptivity.
When a pollen grain reaches the female part of a flower, it has no option but to germinate, creating a pollen tube that grows towards the ovule. In this picture, three pollen tubes are running towards the ovule and one of them has a clear advantage over the others. It may be because it arrived first or because the female part changed its receptivity to accept this specific grain more eagerly than the others.
An intriguing aspect in angiosperm reproduction is the phenomenon of double fertilization. When a pollen grain falls onto the female organ, it germinates, originating a long tube that grows towards the ovule, the so-called pollen tube. The pollen tube carries with it two male gametes: one of them will fertilize the egg cell, giving rise to the zygote that will form the embryo, and the other fertilizes the central cell, an auxiliary cell that accompanies the egg, giving rise to a second zygot that forms the endosperm, a tissue that feeds the embryo during its development.
In the double fertilization of angiosperms, the pollen tube carries two male gametes to the ovule. One of them will fertilize the egg cell, leading to the embryo, and the other will fertilize the central cell, originating the endosperm.
Since the egg and the central cell, as well as both male gametes, are genetically identical, the endosperm is also identical to the embryo and may be seen as an altruist that sacrifices itself to assure the survival of its sibling. The evolutionary origin of the endosperm and its adaptive advantage remain subjects of much discussion and without much solution. The situation is yet more complicated because, in most angiosperms, the endosperm is triploid, having a duplicate maternal material because the central cell has two nuclei. In other words, the endosperm has two copies of the maternal genes and one copy of the paternal genes (configuration 2m/1p), while the embryo is an ordinary organism, having one copy of the maternal genes and one copy of the paternal genes (configuration 1m/1p).
Several hypothesis on the reason that led to the rising of this selfless triploid sibling have been raised and are usually based on different interpretations on the sequence of the events that happened during the evolution of the group. Functionally, the endosperm works are the female gametophyte of other plants, which is, in these, responsible for nourishing the developing embryo. The female gametophyte is the “mother” of the embryo, just like the pollen grain (male gametophyte) is the “father”. The plants with the flowers are, therefore, the embryo’s grandparents. Crazy, isn’t it? But that’s the rule for plants. One generation of large organisms (the sporophyte), gives rise to a generation of tiny organisms (the gametophyte), which in turn will “mate” to generate new large organisms.
Going back to the subject, the functional similarity between the endosperm and the female gametophyte seems to favor the hypothesis that the endosperm was initially a maternal tissue (having, therefore, an original configuration 1m/0p or 2m/0p) and the paternal intromission happened later. On the other hand, the phenomenon of double fertilization is also found in Gnetales (supposedly the closest group to angiosperms) and, in these, double fertilization originates two identical embryos. In addition, basal angiosperms also have diploid endosperms, with a single copy of chromosomes from each parent (1m/1p). This scenario points to a primitive situation of two embryos, in which one of them was deviated to the role of endosperm.
Here we need to include one more important concept in biology: genome imprinting. It is a phenomemon in which genes are differently expressed depending on the parent from which they came; and it is usually seen are a consequence of sexual conflict. What happens is that paternal cells may be silenced in some cells, so that the organism expresses, in those cells, only features inherited through the mothers. The opposite may also happen.
It is assumed that, in angiosperms, the paternal side benefits from the production of large endosperms that provide more nutrients to the embryo, so that there is interest both to express genes leading to a higher accumulation of resources coming from the mother and to silence genes that limit growth. In contrast, the maternal side would attempt to limit the nutrients destined to a single endosperm, as the excess of investment would compromise its future reproductive success. It is better for the mother to invest a little in each endosperm than to invest everything in a single one. Therefore, the maternal side would express genes that control the amount of resources invested in each embryo while inhibiting genes inducing an increased growth.
In such a scenario with genome imprinting, the increased expression of genes by duplication may be seen as a female strategy to counterattack a male attempt to express genes responsible for resource allocation. The paternal plant would express genes for resource collection, while the maternal plant, with two copies of its material in the endosperm, would express genes leading to a contrary response in higher intensity, trying to stop the paternal influence. Such a phenomenon has been attested in corn seeds, where 2m/0p endosperms are smaller than 2m/1p endosperms. As we can see, there is a fight between males and females even among plants!
In angiosperms, fertilization involves the direct interaction of five distinct organisms belonging to three generations: female sporophyte (maternal plant), masculine gametophyte (pollen grain), female gametophyte (ovule), embryo and endosperm. Each one of these organisms has an interest that may be contrary to one or more interests of the others, leading to a complex interaction still poorly defined and in which the endosperm certainly constitutes the most intriguing point and may be the consequence of certain strategies and, at the same time, lead to the emergence of new ones.
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References and further reading:
Alcock J (2001) Animal Behavior, 7th edn. Sinauer Associates, Sunderland
Arnqvist G, Rowe L (2005) Sexual Conflict: Princeton University Press, Princeton, N. J
Baskin, J., & Baskin, C. (2015). Pollen (microgametophyte) competition: an assessment of its significance in the evolution of flowering plant diversity, with particular reference to seed germination Seed Science Research, 25 (01), 1-11 DOI: 10.1017/S0960258515000033
Beale, K., & Johnson, M. (2013). Speed dating, rejection, and finding the perfect mate: advice from flowering plants Current Opinion in Plant Biology, 16 (5), 590-597 DOI: 10.1016/j.pbi.2013.08.005
Becraft, P. (2012). Endosperm Imprinting: A Child Custody Battle? Current Biology, 22 (3) DOI: 10.1016/j.cub.2011.12.043
Cailleau, A., Cheptou, P., & Lenormand, T. (2009). Ploidy and the Evolution of Endosperm of Flowering Plants Genetics, 184 (2), 439-453 DOI: 10.1534/genetics.109.110833
Charnov EL (1979) Simultaneous hermaphroditism and sexual selection. PNAS 76:2480–2484.
Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology, 4th edn. Wiley-Blackwell, Oxford
Dresselhaus, T., & Franklin-Tong, N. (2013). Male–Female Crosstalk during Pollen Germination, Tube Growth and Guidance, and Double Fertilization Molecular Plant, 6 (4), 1018-1036 DOI: 10.1093/mp/sst061
Fetscher AE (2001) Resolution of male-female conflict in an hermaphroditic flower. Proc R Soc B 268:525–529. doi: 10.1098/rspb.2000.1395
Friedman WE (1995) Organismal duplication, inclusive fitness theory, and altruism: understanding the evolution of endosperm and the angiosperm reproductive syndrome. PNAS 92:3913–3917. doi: 10.1073/pnas.92.9.3913
Friedman WE (1998) The evolution of double fertilization and endosperm: an “historical” perspective. Sex Plant Reprod 11:6–16. doi: 10.1007/s004970050114
Friedman WE (2001) Developmental and evolutionary hypotheses for the origin of double fertilization and endosperm. Comptes Rendus de l’Académie des Sciences – Series III – Sciences de la Vie 324:559–567. doi: 10.1016/S0764-4469(01)01326-9
Grossniklaus U, Spillane C, Page DR, Köhler C (2001) Genomic imprinting and seed development: endosperm formation with and without sex. Curr Opin Plant Biol 4:21–27. doi: 10.1016/S1369-5266(00)00130-8
Haig D, Westoby M (1989) Parent-Specific Gene Expression and the Triploid Endosperm. Am Nat 134:147–155.
Haig D, Westoby M (1991) Genomic Imprinting in Endosperm: Its Effect on Seed Development in Crosses between Species, and between Different Ploidies of the Same Species, and Its Implications for the Evolution of Apomixis. Phil Trans R Soc B 333:1–13. doi: 10.1098/rstb.1991.0057
Härdling R, Nilsson P (1999) Parent-Offspring and Sexual Conflicts in the Evolution of Angiosperm Seeds. Oikos 84:27–34. doi: 10.2307/3546863
Lankinen, A., & Madjidian, J. (2011). Enhancing pollen competition by delaying stigma receptivity: Pollen deposition schedules affect siring ability, paternal diversity, and seed production in Collinsia heterophylla (Plantaginaceae) American Journal of Botany, 98 (7), 1191-1200 DOI: 10.3732/ajb.1000510
Leonard JL (1990) The Hermaphrodite’s Dilemma. J Theor Biol 147:361–371. doi: 10.1016/S0022-5193(05)80493-X
Maruyama, D., Hamamura, Y., Takeuchi, H., Susaki, D., Nishimaki, M., Kurihara, D., Kasahara, R., & Higashiyama, T. (2013). Independent Control by Each Female Gamete Prevents the Attraction of Multiple Pollen Tubes Developmental Cell, 25 (3), 317-323 DOI: 10.1016/j.devcel.2013.03.013
Mazer SJ (1987) Maternal investment and male reproductive success in angiosperms: parent-offspring conflict or sexual selection? Biol J Linn Soc 30:115–133. doi: 10.1111/j.1095-8312.1987.tb00293.x
Prasad NG, Bedhomme S (2006) Sexual conflict in plants. J Genet 85:161.
Schärer, L., Janicke, T., & Ramm, S. (2015). Sexual Conflict in Hermaphrodites Cold Spring Harbor Perspectives in Biology, 7 (1) DOI: 10.1101/cshperspect.a017673
Spira TP, Snow AA, Whigham DF, Leak J (1992) Flower Visitation, Pollen Deposition, and Pollen-Tube Competition in Hibiscus moscheutos (Malvaceae). Am J Bot 79:428–433. doi: 10.2307/2445155
Winsor JA, Peretz S, Stephenson AG (2000) Pollen competition in a natural population of Cucurbita foetidissima (Cucurbitaceae). Am J Bot 87:527–532
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