Sequential hermaphroditism

Sequential hermaphroditism (called dichogamy in botany) is a type of hermaphroditism that occurs in many fish, gastropods, and plants. Sequential hermaphroditism occurs when the individual changes sex at some point in its life. It can change from a male to female (protandry), or from female to male (protogyny)[1] or from female to hermaphrodite (protogynous hermaphroditism), or from male to hermaphrodite (protandrous hermaphroditism). Those that change gonadal sex can have both female and male germ cells in the gonads or can change from one complete gonadal type to the other during their last life stage.[2] Individual flowers are also called sequentially hermaphrodite, although the plant as a whole may have functionally male and functionally female flowers open at the same time.

Zoology

Protandry

Ocellaris clownfish, Amphiprion ocellaris, a protandrous animal species

Protandrous hermaphrodites refer to organisms that are born male and at some point in their lifespan change sex to female. Protandrous animals include clownfish. Clownfish have a very structured society. In the Amphiprion percula species, there are zero to four individuals excluded from breeding and a breeding pair living in a sea anemone. Dominance is based on size, the female being the largest and the male being the second largest. The rest of the group is made up of progressively smaller non-breeders, which have no functioning gonads.[3] If the female dies, the male gains weight and becomes the female for that group. The largest non-breeding fish then sexually matures and becomes the male of the group.[4]

Other protandrous fishes can be found in the classes clupeiformes, siluriformes, stomiiformes, and within the perciform families pomacentridae and sparidae. Since these groups are distantly related and have many intermediate relatives that are not protandrous, it strongly suggests that protandry evolved multiple times.[5] Other examples of protandrous animals include:

Protogyny

Moon wrasse, Thalassoma lunare, a protogynous animal species

Protogynous hermaphrodites refer to organisms that are born female and at some point in their lifespan change sex to male. As the animal ages, based on internal or external triggers, it shifts sex to become a male animal. Male fecundity increases greatly with age, unlike female.

Protogyny is the most common form of hermaphroditism in fish in nature.[8] About 75% of the 500 known sequentially hermaphroditic fish species are protogynous.[9][10] Common model organisms for this type of sequential hermaphroditism are wrasses. They are one of the largest families of coral reef fish and belong to the Labridae family. Wrasses are found around the world in all marine habitats and tend to bury themselves in sand at night or when they feel threatened.[11] In wrasses, the larger of the two fish is the male, while the smaller is the female. In most cases, females and immature have a uniform color while the male has the terminal bicolored phase.[12] Large males hold territories and try to pair spawn while small to mid-size initial-phase males live with females and group spawn.[13] In other words, both the initial and terminal phase males can breed; they differ however in the way they do it.

In the California sheephead (Semicossyphus pulcher), a type of wrasse, when the female changes to male, the ovaries degenerate and spermatogenic crypts appear in the gonads. The general structure of the gonads remains ovarian after the transformation and the sperm is transported through a series of ducts on the periphery of the gonad and oviduct. Here sex change is age-dependent. For example, the California sheephead stays a female for four years before changing sex.[12]

Blue-headed wrasse begin life as males or females, but females can change sex and function as males. Young females and males start with a distinct coloration known as the "Initial Phase" before progressing into the "Terminal Phase" coloration, which has a change in intensity of color, stripes, and bars. Initial Phase males have larger testes than larger, terminal phase males, which enables the initial phase males to produce a large amount of sperm. This strategy is able to compete with that of the larger male, who is able to guard his own harem.

Botryllus schlosseri, a colonial tunicate, is a protogynous hermaphrodite. In a colony, eggs are ovulated about two days before the peak of sperm emission.[14] Although self-fertilization is avoided and cross-fertilization favored by this strategy, self-fertilization is still possible. Self-fertilized eggs develop with a substantially higher frequency of anomalies during cleavage than cross-fertilized eggs (23% vs. 1.6%).[14] Also a significantly lower percentage of larvae derived from self-fertilized eggs metamorphose, and the growth of the colonies derived from their metamorphosis is significantly lower. These findings suggest that self-fertilization gives rise to inbreeding depression associated with developmental deficits that are likely caused by expression of deleterious recessive mutations.[15]

Other examples of protogynous organisms include:

Ultimate causes

Ghiselin proposed three models for hermaphroditism in 1969 in his paper titled “The evolution of hermaphroditism among animals”.[21]

  1. The ‘low-density model’ states that individuals have characteristics that reduce the opportunity for mating; this model cannot be applied to sequential hermaphroditism.
  2. The ‘gene dispersal model’ is based on the idea that limitations on dispersal may influence population structure or genetical environment and it can be separated into two versions: the inbreeding version and the sampling-error version. This theory of gene dispersal can be applied to sequential hermaphrodites, especially the inbreeding version. The inbreeding version is based upon the fact that both protandry and protogyny help prevent inbreeding in plants and thus one can make the same assumption that in animals it works by reducing the probability of this occurring among siblings. The sampling-error version is based on the reality that the genetical environment is influenced by genetic drift and similar phenomena in small populations. The two aspects of these hypotheses influenced by hermaphroditism, that is inbreeding and sampling-error, result in the same thing — reduction of genetic variability. In other words, being a hermaphrodite would increase genetic variability and thus be considered advantageous to the population.
  3. Lastly, the ‘size-advantage model’ states that reproductive functions are carried out better if the individual is a certain size/age. To create selection for hermaphroditism, small individuals must have higher reproductive fitness as one sex and larger individuals must have higher reproductive fitness as the opposite sex. With this size-distribution pattern, an individual would maximize its fitness if it reproduced as a sequential hermaphrodite. For example, eggs are larger than sperm, thus if you are a big you are able to make more eggs so being female when big is advantageous, however the size advantage relationship is really not as simple as the example just mentioned, but it allows for a better understanding.

In most ectotherms body size and female fecundity are positively correlated.[1] This supports Ghiselin’s size-advantage model, which is still widely accepted today. Kazancioglu and Alonzo (2010) performed the first comparative analysis of sex change in Labridae. Their analysis supports the size-advantage model by Ghiselin and suggest that sequential hermaphroditism is correlated to the size-advantage. They determined that dioecy was less likely to occur when the size advantage is stronger than other advantages[22]

Warner suggests that selection for protandry may occur in populations where female fecundity is augmented with age and individuals mate randomly. Selection for protogyny may occur where there are traits in the population that depress male fecundity at early ages (territoriality, mate selection or inexperience) and when female fecundity is decreased with age, the latter seems to be rare in the field.[1] An example of territoriality favoring protogyny occurs when there is a need to protect their habitat and being a large male is advantageous for this purpose. In the mating aspect, a large male has a higher chance of mating, while this has no effect on the female mating fitness.[22] Thus, he suggests that female fecundity has more impact on sequential hermaphroditism than the age structures of the population.[1]

The size-advantage model predicts that sex change would only be absent if the relationship between size/age with reproductive potential is identical in both sexes. With this prediction one would assume that hermaphroditism is very common, but this is not the case. Sequential hermaphroditism is very rare and according to scientists this is due to some cost that decreases fitness in sex changers as opposed to those who don’t change sex. Some of the hypotheses proposed for the dearth of hermaphrodites are the energetic cost of sex change, genetic and/or physiological barriers to sex change, and sex-specific mortality rates.[1][23][24]

In 2009, Kazanciglu and Alonzo found that dioecy was only favored when the cost of changing sex was very large. This indicates that the cost of sex change does not explain the rarity of sequential hermaphroditism by itself.[25]

Proximate causes

Many studies have focused on the proximate causes of sequential hermaphroditism. The role of aromatase has been widely studied in this area. Aromatase is an enzyme that controls the androgen/estrogen ratio in animals by catalyzing the conversion of testosterone into oestradiol, which is irreversible. It has been discovered that the aromatase pathway mediates sex change in both directions.[26] Many studies also involve understanding the effect of aromatase inhibitors on sex change. One such study was performed by Kobayashi et al. In their study they tested the role of estrogens in male three-spot wrasses (Halichoeres trimaculatus). They discovered that fish treated with aromatase inhibitors showed decreased gonodal weight, plasma estrogen level and spermatogonial proliferation in the testis as well as increased androgen levels. Their results suggest that estrogens are important in the regulation of spermatogenesis in this protogynous hermaphrodite.[27]

Genetic consequences

Sequential hermaphrodites almost always have a sex ratio biased towards the birth sex, and consequently experience significantly more reproductive success after switching sexes. In theory, this should decrease genetic diversity and effective population size (Ne). However, a study of two ecologically similar santer sea bream (gonochoric) and slinger sea bream (protogynous) in South African waters found that genetic diversities were similar in the two species, and while Ne was lower in the instant for the sex-changer, they were similar over a relatively short time horizion.[28]

Botany

Flowering plants

Protandrous flowers of Aeonium undulatum

In the context of the plant sexuality of flowering plants (angiosperms), there are two forms of dichogamy: protogyny—female function precedes male function—and protandry—male function precedes female function.

Historically, dichogamy has been regarded as a mechanism for reducing inbreeding (e.g., Darwin, 1862). However, a survey of the angiosperms found that self-incompatible (SI) plants, which are incapable of inbreeding, were as likely to be dichogamous as were self-compatible (SC) plants (Bertin, 1993). This finding led to a reinterpretation of dichogamy as a more general mechanism for reducing the impact of pollen-pistil interference on pollen import and export (reviewed in Lloyd & Webb, 1986; Barrett, 2002). Unlike the inbreeding avoidance hypothesis, which focused on female function, this interference-avoidance hypothesis considers both reproductive functions.

In many hermaphroditic species, the close physical proximity of anthers and stigma makes interference unavoidable, either within a flower or between flowers on an inflorescence. Within-flower interference, which occurs when either the pistil interrupts pollen removal or the anthers prevent pollen deposition, can result in autonomous or facilitated self-pollination (Lloyd & Webb, 1986; Lloyd & Schoen, 1992). Between-flower interference results from similar mechanisms, except that the interfering structures occur on different flowers within the same inflorescence and it requires pollinator activity. This results in geitonogamous pollination, the transfer of pollen between flowers of the same individual (Lloyd & Schoen, 1992; de Jong et al., 1993). In contrast to within-flower interference, geitonogamy necessarily involves the same processes as outcrossing: pollinator attraction, reward provisioning, and pollen removal. Therefore, between-flower interference not only carries the cost of self-fertilization (inbreeding depression; Charlesworth & Charlesworth, 1987; Husband & Schemske, 1996), but also reduces the amount of pollen available for export (so-called "pollen discounting"; Harder & Wilson, 1998]). Because pollen discounting diminishes outcross siring success, interference avoidance may be an important evolutionary force in floral biology (Harder & Barrett, 1995, 1996; Harder & Wilson, 1998; Barrett, 2002).

Dichogamy may reduce between-flower interference by minimizing the temporal overlap between stigma and anthers within an inflorescence. Large inflorescences attract more pollinators, potentially enhancing reproductive success by increasing pollen import and export (Schemske, 1980; Queller, 1983; Bell, 1985; Geber, 1985; Schmid-Hempel & Speiser, 1988; Klinkhamer & de Jong, 1990). However, large inflorescences also increase the opportunities for both geitonogamy and pollen discounting, so that the opportunity for between-flower interference increases with inflorescence size (Harder & Barrett, 1996). Consequently, the evolution of floral display size may represent a compromise between maximizing pollinator visitation and minimizing geitonogamy and pollen discounting (Klinkhamer & de Jong, 1993; Barrett et al., 1994; Holsinger, 1996; Snow et al., 1996).

Protandry may be particularly relevant to this compromise, because it often results in an inflorescence structure with female phase flowers positioned below male phase flowers (Bertin & Newman, 1993). Given the tendency of many insect pollinators to forage upwards through inflorescences (Galen & Plowright, 1988), protandry may enhance pollen export by reducing between-flower interference (Darwin, 1862; Harder et al., 2000). Furthermore, this enhanced pollen export should increase as floral display size increases, because between-flower interference should increase with floral display size. These effects of protandry on between-flower interference may decouple the benefits of large inflorescences from the consequences of geitonogamy and pollen discounting. Such a decoupling would provide a significant reproductive advantage through increased pollinator visitation and siring success.

Harder et al. (2000) demonstrated experimentally that dichogamy both reduced rates of self-fertilization and enhanced outcross siring success through reductions in geitonogamy and pollen discounting, respectively. Routley & Husband (2003) examined the influence of inflorescence size on this siring advantage and found a bimodal distribution with increased siring success with both small and large display sizes.

The length of stigmatic receptivity plays a key role in regulating the isolation of the male and female stages in dichogamous plants, and stigmatic receptivity can be influenced by both temperature and humidity.[29] Another study by Jersakova and Johnson, studied the effects of protandry on the pollination process of the moth pollinated orchid, ‘’Satyrium longicauda’’. They discovered that protandry tended to reduce the absolute levels of self-pollination and suggest that the evolution of protandry could be driven by the consequences of the pollination process for male mating success.[30] Another study that indicated that dichogamy might increase male pollination success was the study performed by Dai and Galloway.[31]

See also

References

  1. 1 2 3 4 5 Warner, R.R (1975). "The Adaptive Significance of Sequential Hermaphroditism in Animals.". The American Naturalist. 109: 61–82. doi:10.1086/282974.
  2. ↑ Carruth, L. L (2000). "Freshwater cichlid Crenicara punctulata is a protogynous sequential hermaphrodite". Copeia. 2000: 71–82. doi:10.1643/0045-8511(2000)2000[0071:fccpia]2.0.co;2.
  3. ↑ Buston, P. M (2004). "Territory inheritance in clownfish". Proceedings of the Royal Society B. 271: s252–s254. PMC 1810038 Freely accessible. PMID 15252999. doi:10.1098/rsbl.2003.0156.
  4. ↑ Buston, P (2004). "Does the Presence of Non-Breeders Enhance the Fitness of Breeders ? An Experimental Analysis in the Clown Anemonefish Amphiprion percula". Behavioral Ecology and Sociobiology. 57: 23–31. doi:10.1007/s00265-004-0833-2.
  5. ↑ Avise, J.C.; Mank, J.E. (2009). "Evolutionary Perspectives on Hermaphroditism in Fishes". Sexual Development. 3 (2–3): 152–163. doi:10.1159/000223079.
  6. 1 2 Policansky, D (1982). "Sex change in plants and animals". Annual Review of Ecology and Systematics. 13: 471–495. doi:10.1146/annurev.es.13.110182.002351.
  7. ↑ Russell-Hunter, W. D.; McMahon, R. F. (1976). "Evidence for functional protandry in a fresh-water basommatophoran limpet, Laevapex fuscus". Transactions of the American Microscopical Society. 95 (2): 174–182. JSTOR 3225061. doi:10.2307/3225061.
  8. ↑ Avise, JC; JE Mank (2009). "Evolutionary Perspectives on Hermaphroditism in Fishes". Sexual Development. 3: 152–163. doi:10.1159/000223079.
  9. ↑ Pauly, Daniel (2004). Darwin's Fishes: An Encyclopedia of Ichthyology, Ecology, and Evolution. Cambridge University Press. p. 108. ISBN 9781139451819.
  10. ↑ Pandian, TJ (2012). Genetic Sex Differentiation in Fish. Boca Raton, FL: Science Publishers.
  11. ↑ "Animal Planet :: Fish Guide -- Wrasse". PetEducation.com. Retrieved 2011-03-28.
  12. 1 2 Warner, R.R (1975). "The reproductive biology of the Protogynous hermaphrodite Pimelometopon Pulchrum (Pisces: Labridae).". Fishery Bulletin. 73: 261–283.
  13. ↑ Adreani, M S; L G Allen (2008). "Mating system and reproductive biology of a temperate wrasse, Halichoeres semicinctus". Copeia. 2008: 467–475. doi:10.1643/cp-06-265.
  14. 1 2 Gasparini F; Manni L; Cima F; Zaniolo G; Burighel P; Caicci F; Franchi N; Schiavon F; Rigon F; Campagna D; Ballarin L (July 2014). "Sexual and asexual reproduction in the colonial ascidian Botryllus schlosseri". Genesis. 53: 105–20. PMID 25044771. doi:10.1002/dvg.22802.
  15. ↑ Bernstein, H; Hopf, FA; Michod, RE (1987). "The molecular basis of the evolution of sex". Adv Genet. 24: 323–70. PMID 3324702. doi:10.1016/S0065-2660(08)60012-7.
  16. ↑ "Familie Serranidae - Sea basses: groupers and fairy basslets". Fishbase. August 26, 2010. Retrieved January 21, 2012.
  17. ↑ "Anthiinae - the Fancy Basses". Reefkeeping Magazine. 2008. Retrieved January 21, 2012.
  18. ↑ R. Thompson & J.L. Munro (1983). "The Biology, Ecology and Bionomics of the Hinds and Groupers, Serranidae". In J. L. Munro. Caribbean Coral Reef Fishery Resources. The WorldFish Center. p. 62. ISBN 978-971-10-2201-3.
  19. ↑ J.R. Gold (1979). "Cytogenetics". In W.S. Hoar; D.J. Randall; J.R. Brett. Bioenergetics and Growth. Fish Physiology. VIII. Academic Press. p. 358. ISBN 978-0-12-350408-1.
  20. ↑ Dimitri A. Pavlov; Natal'ya G. Emel'yanova & Georgij G. Novikov (2009). "Reproductive Dynamics". In Tore Jakobsen; Michael J. Fogarty; Bernard A. Megrey & Erlend Moksness. Fish Reproductive Biology: Implications for Assessment and Management. John Wiley and Sons. p. 60. ISBN 978-1-4051-2126-2.
  21. ↑ Ghiselin, M T (1969). "The evolution of hermaphroditism among animals". The Quarterly Review of Biology. 44 (2): 189–208. PMID 4901396. doi:10.1086/406066.
  22. 1 2 Kazancioğlu, E; SH Alonzo (2010). "A comparative analysis of sex change in Labridae supports the size advantage hypothesis". Evolution; international journal of organic evolution. 64 (8): 2254–64. PMID 20394662. doi:10.1111/j.1558-5646.2010.01016.x.
  23. ↑ Charnov, E (1986). "Size Advantage May Not Always Favor Sex Change". Journal of Theoretical Biology. 119: 283–285. doi:10.1016/s0022-5193(86)80141-2.
  24. ↑ Munday, P; BW Molony (2002). "The energetic cost of protogynous versus protandrous sex change in the bi-directional sex changing fish Gobiodon histrio". Marine Biology. 141: 429–446. doi:10.1007/s00227-002-0904-8.
  25. ↑ Kazancioğlu, E; SH Alonzo (2009). "Costs of changing sex do not explain why sequential hermaphroditism is rare". The American Naturalist. 173 (3): 327–36. PMID 19199519. doi:10.1086/596539.
  26. ↑ Kroon, FJ; Munday, P. L.; Westcott, D.; Hobbs, J.-P.; Liley, N. R. (2005). "Aromatase pathway mediates sex change in each direction.". Proceedings of the Royal Society B. 272 (1570): 1399–405. PMC 1560338 Freely accessible. PMID 16006326. doi:10.1098/rspb.2005.3097.
  27. ↑ Kobayashi, y; Nozu R; Nakamura M. (2011). "Role of estrogen in spermatogenesis in initial phase males of the three-spot wrasse (Halichoeres trimaculatus): wffect of aromatase inhibitor on the testis.". Developmental Dynamics. 240: 116–121. PMID 21117145. doi:10.1002/dvdy.22507. Retrieved 2011-04-27.
  28. ↑ Coscia, I; Chopelet, J; Waples, R S; Mann, B Q; Mariani, S (2016). "Sex change and effective population size: implications for population genetic studies in marine fish". Heridity. 117: 251–258. doi:10.1038/hdy.2016.50.
  29. ↑ Lora, J; Herrero, M.; Hormaza, J. I. (2011). "Stigmatic receptivity in a dichogamous early-divergent angiosperm species, Annona cherimola (Annonaceae): Influence of temperature and humidity.". American Journal of Botany. 98: 265–274. PMID 21613115. doi:10.3732/ajb.1000185. Retrieved 2011-04-27.
  30. ↑ Jersáková, J; SD Johnson (2007). "Protandry promotes male pollination success in a moth-pollinated orchid.". Functional Ecology. 21: 496–504. doi:10.1111/j.1365-2435.2007.01256.x. Retrieved 2011-04-27.
  31. ↑ Dai, C; L F Galloway (2011). "Do dichogamy and herkogamy reduce sexual interference in a self-incompatible species?". Functional Ecology. 25: 271–278. doi:10.1111/j.1365-2435.2010.01795.x. Retrieved 2011-03-28.

Further reading

  • Barrett SC (February 2002). "Sexual interference of the floral kind". Heredity. 88 (2): 154–9. PMID 11932774. doi:10.1038/sj.hdy.6800020. 
  • Barrett, S.C.H., Harder, L.D., Cole W.W. (1994). "Effects of Flower Number and Position on Self-Fertilization in Experimental Populations of Eichhornia paniculata (Pontederiaceae)". Functional Ecology. 8 (4): 526–35. JSTOR 2390078. doi:10.2307/2390078. 
  • Bell G. (1985). "On the function of flowers". Proceedings of the Royal Society B. 224: 223–65. doi:10.1098/rspb.1985.0031. 
  • Bertin, R.I. (1993). "Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms". Amer. J. Bot. 80 (5): 557–60. JSTOR 2445372. doi:10.2307/2445372. 
  • Bertin R.I.; Newman C.M. (1993). "Dichogamy in angiosperms". Bot. Rev. 59: 112–52. doi:10.1007/BF02856676. 
  • Darwin, Charles (1862). On the various contrivances by which British and foreign orchids are fertilized by insects, and on the good effects of intercrossing. London: John Murray. 
  • Charlesworth, D., Charlesworth, B. (1987). "Inbreeding Depression and its Evolutionary Consequences". Annual Review of Ecology and Systematics. 18: 237–68. JSTOR 2097132. doi:10.1146/annurev.es.18.110187.001321. 
  • de Jong, T.J., Waser, N.M., Klinkhamer, P.G.L. (1993). "Geitonogamy: the neglected side of selfing". Trends Ecol. Evol. 8: 321–25. doi:10.1016/0169-5347(93)90239-L. 
  • Galen, C., Plowright, R.C. (1988). "Contrasting movement patterns of nectar-collecting and pollen-collecting bumble bees (Bombus terricola) on fireweed (Chamaenerion angustifolium) inflorescences". Ecol. Entomol. 10: 9–17. doi:10.1111/j.1365-2311.1985.tb00530.x. 
  • Geber, M. (1985). "The Relationship of Plant Size to Self-Pollination in Mertensia ciliata". Ecology. 66 (3): 762–72. JSTOR 1940537. doi:10.2307/1940537. 
  • Griffin SR; Mavraganis K; Eckert CG (September 2000). "Experimental analysis of protogyny in Aquilegia canadensis (Ranunculaceae)". American Journal of Botany. 87 (9): 1246–1256. JSTOR 2656717. PMID 10991895. doi:10.2307/2656717. 
  • Harder, L.D., Barrett, S.C.H. (February 1995). "Mating cost of large floral displays in hermaphrodite plants". Nature. 373 (6514): 512–5. doi:10.1038/373512a0. 
  • Harder, L.D., Barrett, S.C.H. (1996). "Pollen dispersal and mating patterns in animal-pollinated plants". In Lloyd, D.G.; Barrett, S.C.H. Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants. NY: Chapman & Hall. pp. 140–190. 
  • Harder, L.D., Wilson, W.G. (November 1998). "A Clarification of Pollen Discounting and Its Joint Effects with Inbreeding Depression on Mating System Evolution". The American Naturalist. 152 (5): 684–95. JSTOR 2463846. PMID 18811343. doi:10.1086/286199. 
  • Harder LD; Barrett SC; Cole WW (February 2000). "The mating consequences of sexual segregation within inflorescences of flowering plants". Proceedings of the Royal Society B. 267 (1441): 315–20. PMC 1690540 Freely accessible. PMID 10722210. doi:10.1098/rspb.2000.1002. 
  • Holsinger K.E. (1996). "Pollination biology and the evolution of mating systems in flowering plants". In Hecht, M.K. Evolutionary Biology. NY: Plenum Press. pp. 107–149. 
  • Husband, B.C., Schemske D.W. (February 1996). "Evolution of the Magnitude and Timing of Inbreeding Depression in Plants". Evolution. 50 (1): 54–70. JSTOR 2410780. doi:10.2307/2410780. 
  • Klinkhamer, P.G.L., de Jong, T.J. (1990). "Effects of plant size, plant density and sex differential nectar reward on pollinator visitation in the protandrous Echium vulgare". Oikos. 57 (3): 399–405. JSTOR 3565970. doi:10.2307/3565970. 
  • Klinkhamer, P.G.L., de Jong, T.J. (1993). "Attractiveness to pollinators: a plant’s dilemma". Oikos. 66 (1): 180–4. JSTOR 3545212. doi:10.2307/3545212. 
  • Lloyd, D.G., Webb, C.J. (1986). "The avoidance of interference between the presentation of pollen and stigmas in angiosperms: I. Dichogamy". New Zeal. J. Bot. 24: 135–62. doi:10.1080/0028825x.1986.10409725. 
  • Lloyd, D.G., Schoen D.J. (September 1992). "Self- and Cross-Fertilization in Plants. I. Functional Dimensions". International Journal of Plant Sciences. 153 (3, Part 1): 358–69. doi:10.1086/297040. 
  • Queller, D.C. (1983). "Sexual selection in a hermaphroditic plant". Nature. 305 (5936): 706–7. doi:10.1038/305706a0. 
  • Routley MB; Husband BC (February 2003). "The effect of protandry on siring success in Chamerion angustifolium (Onagraceae) with different inflorescence sizes". Evolution. 57 (2): 240–8. PMID 12683521. doi:10.1554/0014-3820(2003)057[0240:teopos]2.0.co;2. 
  • Schemske, D.W. (1980). "Evolution of floral display in the orchid Brassavola nodosa". Evolution. 34 (3): 489–91. JSTOR 2408218. doi:10.2307/2408218. 
  • Schmid-Hempel, P., Speiser, B. (1988). "Effects of inflorescence size on pollination in Epilobium angustifolium". Oikos. 53 (1): 98–104. JSTOR 3565669. doi:10.2307/3565669. 
  • Snow, A.A., Spira, T.P., Simpson, R., Klips, R.A. (1996). "The ecology of geitonogamous pollination". In Lloyd, D.G.; Barrett, S.C.H. Floral Biology: Studies on Floral Evolution in Animal-Pollinated Plants. NY: Chapman & Hall. pp. 191–216. 
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