×

Hermaphroditism: What’s not to like? (English) Zbl 1451.92221

Summary: Hermaphroditism is rare and phylogenically in decline among animal species. The evolutionary basis for this development is not well understood. This paper focusses on self-incompatible simultaneous hermaphroditism in animals. It proposes that such hermaphroditism is not stable in sufficiently heterogeneous populations, suggesting a possible reason for why hermaphroditism is rare among evolved animal species. The argument turns on the Bateman principle, namely that male reproductive success (RS) is limited by partner availability, while female RS is not. We show that: low-quality individuals do better if female; secondary sexual differentiation may be important for understanding the existence of males; and that hermaphroditic mating is reciprocal. Reciprocity may be key to understanding promiscuity and attendant phenomena such as cryptic female choice, sperm competition and love darts – common features of hermaphroditic mating. We also argue that hermaphrodites are especially vulnerable to male violence, suggesting a reason for the rarity of trioecy. Finally, we propose that external fertilization, and the scope for streaking, may be one reason fish are the only simultaneously hermaphroditic vertebrates.

MSC:

92D15 Problems related to evolution

References:

[1] Charnov, E. L., Simultaneous hermaphroditism and sexual selection, Proc. Natl Acad. Sci. USA, 76, 5, 2480-2484 (1979)
[2] Charnov, E. L., The Theory of Sex Allocation (1982), Princeton University Press: Princeton University Press Princeton, NJ
[3] Charnov, E. L.; Maynard Smith, J.; Bull, J. J., Why be an hermaphrodite?, Nature, 263, 5573, 125-126 (1976)
[4] Charnov, E. L.; Los den Hartogh, R. L.; Jones, W. T.; van den Assem, J., Sex ratio evolution in a variable environment, Nature, 289, 5793, 27-33 (1981)
[5] DeWitt, T. J., Gender contests in a simultaneous hermaphrodite snail: a size-advantage model for behaviour, Anim. Behav., 51, 2, 345-351 (1996)
[6] Fischer, E. A., The relationship between mating system and simultaneous hermaphroditism in the coral-reef fish, Hypoplectrus-Nigricans (Serranidae), Anim. Behav., 28, 620-633 (1980)
[7] Ghiselin, M. T., The evolution of hermaphroditism among animals, Q. Rev. Biol., 47, 189-208 (1969)
[8] Greeff, J. M.; Michiels, N. K., Low potential for sexual selection in simultaneously hermaphroditic animals, Proc. R. Soc. London, 266, 1671-1676 (1999)
[9] Greeff, J. M.; Michiels, N. K., Sperm digestion and reciprocal sperm transfer can drive hermaphrodite sex allocation to equality, Am. Nat., 153, 4, 421-430 (1999)
[10] Haase, M.; Karlsson, A., Mate choice in a hermaphrodite: you won’t score with a spermatophore, Anim. Behav., 67, 2, 287-291 (2004)
[11] Hurst, L.; Hamilton, W., Cytoplasmic fusion and the nature of sexes, Proc. R. Soc., 1320, 247, 189-207 (1992)
[12] Leonard, J. L.; Lukowiak, K., Male-female conflict in a simultaneous hermaphrodite resolved by sperm-trading, Am. Nat., 124, 2, 282-286 (1984)
[13] Lüscher, A.; Wedekind, C., Size-dependent discrimination of mating partners in the simultaneous hermaphroditic cestode Schistocephalus solidus, Behav. Ecol., 13, 2, 254-259 (2002)
[14] Maynard Smith, J., The Evolution of Sex (1978), Cambridge University Press: Cambridge University Press Cambridge
[15] Michiels, N. K.; Newman, L. J., Sex and violence in hermaphrodites, Nature, 391, 6668, 647 (1998)
[16] Michiels, N. K.; Streng, A., Sperm exchange in a simultaneous hermaphrodite, Behav. Ecol. Sociobiol., 42, 3, 171-178 (1998)
[17] Michiels, N. K.; Hohner, A.; Vorndran, I. C., Precopulatory mate assessment in relation to body size in the earthworm Lumbricus terrestris: avoidance of dangerous liaisons?, Behav. Ecol., 12, 5, 612-618 (2001)
[18] Oliver, A. S., Size and density dependent mating tactics in the simultaneously hermaphroditic seabass Serranus subligarius (cope, 1870), Behaviour, 134, 7-8, 563-594 (1997)
[19] Petersen, C. W., Reproductive-behavior, egg trading, and correlates of male mating success in the simultaneous hermaphrodite, Serranus-tabacarius, Environ. Biol. Fishes, 43, 4, 351-361 (1995)
[20] Petersen, C. W., Sexual selection and reproductive success in hermaphroditic seabasses, Integrative Comp. Biol., 46, 4, 439-448 (2006)
[21] Sella, G., Reciprocal egg trading and brood care in a hermaphroditic polychaete worm, Anim. Behav., 33, 3, 938-944 (1985)
[22] Sella, G.; Lorenzi, M. C., Partner fidelity and egg reciprocation in the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema, Behav. Ecol., 11, 3, 260-264 (2000)
[23] Sella, G.; Premoli, M. C.; Turri, F., Egg trading in the simultaneously hermaphroditic polychaete worm Ophryotrocha gracilis (Huth), Behav. Ecol., 8, 1, 83-86 (1997)
[24] St. Mary, C. M., Sex allocation in a simultaneous hermaphrodite, the blue-banded goby (Lythrypnus dalli): the effects of body size and behavioral gender and the consequences for reproduction, Behav. Ecol., 5, 3, 304-313 (1994)
[25] Trivers, R. L.; Willard, D. E., Natural selection of parental ability to vary the sex-ratio of offspring, Science, 179, 90-92 (1973)
[26] Weeks, S.C., Sanderson, T.F., Reed, S.K., Zofkova, M., Knott, B., Balaraman, U., Pereira, G., Senyo, D.M., Hoeh, W.R., 2006. Ancient androdioecy in the freshwater crustacean Eulimnadia. Proc. R. Soc. London Ser. B 273 (1587), 725-734.
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.