Evolutionary Perspectives on Hermaphroditism in Fishes

Evolutionary Perspectives on Hermaphroditism in Fishes

Review Article Sex Dev 2009;3:152–163 Received: July 18, 2008 DOI: 10.1159/000223079 Accepted: September 22, 2008 Evolutionary Perspectives on Hermaphroditism in Fishes a b J.C. Avise J.E. Mank a Department of Ecology and Evolutionary Biology, University of California, Irvin e, Calif. , USA b Department of Zoology, University of Oxford, Oxford , UK Key Words The ancient Greeks were intrigued in their mytholo- -Mating systems ؒ Outcrossing ؒ Phylogenetics ؒ gies by the concept of hermaphroditism, i.e. the expres Self-fertilization ؒ Sexual systems sion of both male and female sex within the lifetime of an individual (Box 1). Hermaphroditism also intrigues mod- ern biologists, for several reasons: many real-world plants Abstract and animals exhibit the phenomenon [Policansky, 1982]; Hermaphroditism is a derived and polyphyletic condition in it is so obviously different from the typical human condi- fishes, documented in about 2% of all extant teleost spe- tion of distinct lifelong sexes; and the adaptation raises cies scattered across more than 20 taxonomic families in 9 many interesting evolutionary questions and scenarios. orders. It shows a variety of expressions that can be cat- In fishes, either simultaneous or sequential hermaphro- egorized into sequential and synchronous modes. Among ditism has been documented in approximately 500 (2%) the sequential hermaphrodites are protogynous species in of 25,000 extant species [Pauly, 2004] representing more which an individual begins reproductive life as a female and than 20 taxonomic families in 9 orders [Breder and Rosen, later may switch to male, protandrous species in which a fish 1966; Smith, 1975; Mank et al., 2006]. Sexual differentia- starts as a male and later may switch to female, and serial bi- tion in fishes thus is evolutionarily quite labile as well as directional sex changers. Among the synchronous hermaph- developmentally plastic. rodites (in which an individual can simultaneously produce eggs and sperm) are several outcrossing and one predomi- nantly selfing species. A few species also consist of mixtures Box 1. Hermaphroditism in Greek Mythology of hermaphroditic and single-sex individuals. All of these re- productive categories have been the subject of numerous The word hermaphrodite derives from the Greek theoretical and empirical treatments from an evolutionary myth of Hermaphroditos, a handsome son of Hermes perspective. Here we highlight some of the major con- and Aphrodite, the Greek gods of male and female sex- clusions from these studies, which collectively have been uality. At age 15, Hermaphroditos was accosted one day informative on a variety of biological topics related to re- by a lovely nymph – Salmacis – who embraced him, productive modes, gender allocations, sexual conflict and kissed him, and prayed to the gods that they be united gamesmanship, mating systems, and life-history tradeoffs. forever. Her wish was granted and Hermaphroditos Copyright © 2009 S. Karger AG, Basel thereafter became simultaneously part male and part © 2009 S. Karger AG, Basel John C. Avise 1661–5425/09/0033–0152$26.00/0 Department of Ecology and Evolutionary Biology Fax +41 61 306 12 34 University of California E-Mail [email protected] Accessible online at: Irvine, CA, 92697 (USA) www.karger.com www.karger.com/sxd Tel. +1 949 824 3925, Fax +1 949 824 2181, E-Mail [email protected] Hermaphroditism Gonochorism Protandrous Protogynous Simultaneous Beloniformes × Cyprinodontiformes × × × Atheriniformes × Perciformes × Synbranchiformes × × Perciformes × Pleuronectiformes × Perciformes × × × × Tetraodontiformes × Gasterosteiformes × Scorpaeniformes × Stephanoberyciformes × Beryciformes × Zeiformes × Myctophiformes × Aulopiformes × × Stomiiformes × × Fig. 1. Distributions of various types of Salmoniformes × hermaphroditism (male-first or protan- Characiformes × drous, female-first or protogynous, and si- Gymnotiformes × multaneous) and gonochorism (separate Siluriformes × × sexes), along extant nodes of a provisional supertree for bony fishes [after Mank et Cypriniformes × × al., 2006]. The supertree is a cladogram Clupeiformes × × (branch lengths are not proportional to di- Anguilliformes × × × vergence time) that represents an amalga- Osteoglossiformes × mation of several published phylogenies Acipenseriformes × from whole-genome or partial-genome mtDNA sequences. Note that ‘Perciformes’ Rajiformes × is polyphyletic. female. Tiresias – the blind prophet-priest of Zeus – roditism. For example, Moe [1969] suggested that se- was another type of hermaphrodite who in this case quential hermaphroditism might have evolved as a popu- switched sequentially between male and female. It all lation control mechanism, with the age of transformation began when Tiresias chanced upon a pair of copulating between female and male shifting up or down to compen- snakes and beat them with a stick. Hera (the wife of sate for whether a population was too sparse or too dense. Zeus) was infuriated, and punished Tiresias by trans- Other hypotheses with a group-selection aura posited forming him into a woman. Seven years later, Tiresias that hermaphroditism might increase total zygotic pro- again encountered two mating snakes, but this time left duction in a population [Smith, 1967] or focus sexual per- the serpents alone. As a reward, Hera permitted Tire- formances into age classes that would maximize a popu- sias to regain a male condition. lation’s reproductive output [Nikolski, 1963]. By contrast, more modern views have emphasized Earlier researchers sometimes invoked population- how natural selection and sexual selection might operate, level advantages to rationalize the evolution of hermaph- in various social and ecological contexts, on the differen- Hermaphroditism in Fish Sex Dev 2009;3:152–163 153 phic for reproductive mode indicates that each hermaph- Leuciscus roditic clade typically is embedded within a deeper clade otherwise composed of gonochoristic taxa (example in Scardinius fig. 2 ). Extant hermaphroditism in teleost fish is therefore Phoxinus a polyphyletic and derived condition relative to gonocho- Cyprinidae rism. Furthermore, no extant hermaphroditic lineage ap- Carassius pears to be evolutionarily ancient (although this should be interpreted in light of the fact that no single sex deter- Cyprinus mining mechanism in fish appears to be ancient [Mank et al., 2006], and thus need not imply that hermaphrodit- Barbus ism is any less evolutionarily stable than alternative strat- egies). The evolutionary flexibility of reproductive modes Lepidocephalichthys in fishes also extends to different forms of hermaphro- Cobitidae ditism ( figs. 1 , 3 ), including female-first protogyny and Cobitis male-first protandry (see beyond). Transitional States . Far less certain, however, are an- swers to the following questions. How exactly does her- Fig. 2. Phylogenetic position of protogynous hermaphroditism (open branches) within cypriniform fishes [after Mank et al., maphroditism evolve from gonochorism? And, does 2006]. Filled branches reflect gonochorism. gonochorism ever re-emerge from phylogenetically lo- calized instances of ancestral hermaphroditism? Some insight can be gleaned from the plant literature, where theoretical and empirical methods have been used to elu- tial fitnesses of individuals who have the capacity to re- cidate the evolutionary history of hermaphroditism. In produce as males and females at various stages of life principle, gonochorism and synchronous hermaphrodit- [Warner, 1975; Shapiro, 1987; Leonard, 2006]. Addition- ism are evolutionary endpoints on a reproductive spec- ally, there are several different types of hermaphroditism, trum that includes intermediate mixed-sex modalities which can be broadly categorized by whether each indi- ( fig. 4 ): gynodioecy (a population mixture of females and vidual in a species produces male and female gametes si- hermaphrodites), androdioecy (a mixture of males and multaneously (like Hermaphroditos; see Box 1) or wheth- hermaphrodites), and trioecy (males, females, and her- er it switches sex during life but has only one functional maphrodites). Trioecy is extremely rare in the biological sex at any time (like Tiresias; see Box 1). Alternative types world and androdioecy is only slightly less so [Weeks et of hermaphroditism have different evolutionary paths, al., 2006], but gynodioecy is rather common (especially and modern evolutionary theory has identified some of in plants, where 1 500 species in 50 families display the the causes and implications. phenomenon) [Jacobs and Wade, 2003]. Theoretical This review will encapsulate major conclusions – from models addressing these biological patterns (again, pri- previous empirical studies and theoretical treatments marily in plants) have a long history [Lloyd, 1975; Charles- about the evolution of hermaphroditism in fishes. Endo- worth and Charlesworth, 1978; Charnov, 1982; Charles- crinological, physiological, and other ontogenetic me- worth, 1984; Barrett, 1998; Jarne and Charlesworth, 1993; chanics of sex change are also of scientific interest, but Pannell, 2000; Wolf and Takebayashi, 2004], and they these are addressed elsewhere [see Nakamura et al., 2005] generally suggest the following. and will not be the focus here. During an evolutionary transition between separate- sex and purely hermaphroditic reproduction, typically Evolutionary History one sex at a time is either lost (in a transition from gono- Phylogenetic Backdrop . The 9 taxonomic orders of tel- chorism to hermaphroditism)

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