vol. 183, no. 4 the american naturalist april 2014

Sexual Dimorphism in Body Size and the Origin of Sex-Determination Systems

Elizabeth Adkins-Regan1,2,* and Hudson K. Reeve2

1. Department of Psychology, Cornell University, Ithaca, New York 14853; 2. Department of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853 Submitted March 26, 2013; Accepted October 10, 2013; Electronically published February 26, 2014

type XY (Graves 2008), and teleost fishes, urodele am- abstract: Diverse sex-determining systems occur in vertebrates, phibians, and anuran amphibians all include both types including environmental sex determination (ESD), genetic sex de- termination (GSD) of type XX/XY (heterogametic males), and GSD (Hillis and Green 1990; Klinkhardt et al. 1995; Schmid of type ZZ/ZW (heterogametic females). The origins of the two ge- and Steinlein 2001; Devlin and Nagahama 2002). netic types are poorly understood. We use protected invasion theory The phylogenetic distribution of these sex-determining to derive a model that generates testable predictions about the origins systems and types is striking. Some vertebrate groups, such of the two genetic types from ESD. Protected invasion theory predicts as snakes, birds, or mammals, are very homogeneous. In biases in the evolutionary origins of new traits by focusing on the these groups, all sex determination is genetic, and it is probability that a selectively favored trait will avoid loss by genetic always of the same (or very similar) type. Others, such as drift when rare. We show that the theory makes predictions about the conditions under which XY or ZW systems are more likely to amphibians, scincomorph and gekkomorph lizards, and arise from an ancestral state of ESD. In particular, assuming that teleost fishes, are heterogeneous. In these groups, variation there is an average trend toward increasing body size in lineages, the in the type of GSD (XY or ZW) is seen within families, origins of XY systems are predicted to be accompanied by increases genera, and even species. Across all vertebrates, the phy- in male : female body size ratio. In contrast, ZW systems are predicted logenetic distribution of sex-determining systems suggests to be accompanied by decreases in male : female body size ratio. We multiple independent evolutionary origins and reversals find support for these predictions in the form of a marked association (Mank et al. 2006; Ezaz et al. 2009). among vertebrates between sex-determining system and body size dimorphism in paired comparisons independent of shared phylogeny. There have been numerous reviews of sex-determining systems in vertebrates aimed at understanding their evo- lution, including more than a dozen since 2000 (e.g., Kraak Keywords: genetic sex determination, environmental sex determi- nation, evolutionary origin, protected invasion theory, comparative and Pen 2002; Mank et al. 2006; Graves 2008). Under- analysis, size dimorphism. standing the phylogeny of sex-determining systems re- quires two kinds of investigation. One type addresses how there can be so much diversity by uncovering the genetic Introduction changes underlying origins of new systems and transitions from one system to another. The other type addresses why Vertebrate sex-determining systems are diverse (fig. 1). Sex there is so much diversity by investigating the selective can be determined by the physical or social environment, pressures and fitness consequences of the different systems by genes, or by both environment and genes operating (Trivers 1988; Werren and Beukeboom 1998). Consider- together. Genetic sex determination (GSD) can be either able progress has been made using population genetics of the XX/XY type (male heterogamety, hereafter XY) or and other tools to model the sequence of changes that the ZZ/ZW type (female heterogamety, hereafter ZW). would have to occur for XY GSD to change to ZW GSD More than 2,000 species, including some sharks and rays, and vice versa (Bull 1983; Quinn et al. 2011). This has have been shown to have GSD, and many others have helped explain how such changes have been able to occur 1 : 1 offspring sex ratios suggestive of GSD (Maddock and multiple times in vertebrates—that is, how such diversity Schwartz 1996). Birds and snakes exclusively have type has been genetically possible (Werren and Beukeboom ZW (Janzen and Paukstis 1991), mammals exclusively have 1998). Models of the evolution of one GSD type from * Corresponding author; e-mail: [email protected]. another have highlighted the potential roles of sex-ratio Am. Nat. 2014. Vol. 183, pp. 519–536. ᭧ 2014 by The University of Chicago. selection or sex-antagonistic selection (Bull 1983; Uller et 0003-0147/2014/18304-54571$15.00. All rights reserved. al. 2007; Pen et al. 2010; van Doorn and Kirkpatrick 2010). DOI: 10.1086/675303 Progress has also been made in explaining why the chro- 520 The American Naturalist

Ray-finned fishes: ESD, XY, ZW receive empirical support (Janzen and Phillips 2006; Crews and Bull 2008; Warner and Shine 2008). What is still inadequately explained is what selective pressures determine which GSD system will evolve. What are the evolutionary origin mechanisms that bias a lineage Amphibians: XY, ZW toward GSD of one type over another? That evolutionary change happens and happens readily is now less of a ge- netic mystery. But what accounts for when and where the changes have occurred in the evolution of vertebrates? Mammals: XY Explaining the current distribution of GSD types in ver- tebrates continues to represent a major challenge, one that has seldom been addressed (see next section for the im- portant exceptions, i.e., the work of Kraak and de Looze [1993] and Kraak and Pen [2002]). Snakes: ZW This article presents a model derived from protected invasion theory (Reeve 1993; Reeve and Shellman-Reeve 1997) that generalizes the predictions of Kraak and de Looze (1993) about the evolution of the two GSD types Lizards: XY, ZW, ESD from ESD. The model generates a prediction that GSD type will be associated with sexual size dimorphism. This is tested with reference to those vertebrates most likely to have an ESD origin for their sex-determining systems. Turtles: ESD, XY, ZW

Prior Models for the Evolution of GSD from ESD

Since Bull’s (1983) comprehensive review of models for Crocodiles: ESD the evolution of GSD from ESD, few additional formal models have been proposed (Kraak and de Looze 1993; Kraak and Pen 2002; Van Dooren and Leimar 2003; Pen et al. 2010; Quinn et al. 2011). The first and only extant Birds: ZW model that explicitly predicts an association with body size dimorphism is that of Kraak and de Looze (1993). In reptiles, ESD by temperature-dependent sex deter- Figure 1: Diversity in sex-determining systems among and within mination (TSD) and body size dimorphism are associated, p major vertebrate clades. ESD environmental sex determination; such that differentiation of females at higher incubation XY p genetic sex determination of the XX/XY type (male hetero- gamety); ZW p genetic sex determination of the ZZ/ZW type (fe- temperatures is associated with larger female body size male heterogamety). relative to males (Type I TSD, as in many turtles), whereas differentiation of males at higher incubation temperatures is associated with larger male body size relative to females mosome with the sex-determining gene(s) on it tends to (Type II TSD, as in Crocodylia and Eublepharis lizards; become reduced in size (i.e., why sex chromosomes be- Deeming and Ferguson 1991; Ewert et al. 1994; Viets et come heteromorphic), why it might be difficult for GSD al. 1994). Building on Charnov and Bull’s (1977) model type to change once this happens, and why strong chro- for explaining ESD as a consequence of a sex difference mosomal heteromorphism leads to fixation of XY or ZW, in the relation between body size and fitness and Mitt- as in mammals, snakes, and birds (Bull 1983; Charlesworth woch’s (1971) mechanistic proposal that rate of gonadal 1991; Rice 1994; Graves 1995; Charlesworth et al. 2005). growth determines gonadal sex, Kraak and de Looze (1993) Some authors have mapped known sex-determining sys- proposed that in ESD species, a chromosome with a mu- tems onto modern phylogenies, allowing reconstruction tation causing females to grow faster would eventually of the most likely ancestral states (e.g., Hillis and Green become a W (i.e., a ZW system would be favored by a 1990; Kraak and Pen 2002; Janzen and Phillips 2006). female size advantage) and one with a mutation causing Theories for the evolution of temperature-dependent en- males to grow faster would become a Y (i.e., an XY system vironmental sex determination (ESD) are beginning to would be favored by a fitness advantage of male size). A Origin of Sex-Determination Systems 521 multilocus formal version of the model was later developed test the prediction with data on GSD systems in (Kraak and Pen 2002). vertebrates. The empirical evidence presented in Kraak and de Looze (1993) for their predicted relationship between a sex dif- ference in size advantage and sex-determining system was Protected Invasion Theory and the that in four species of reptiles with ESD (three turtles and Evolution of GSD from ESD the American alligator), H-Y antigen is detected in the larger sex. H-Y antigen is a male histocompatibility antigen If bearers of a new favored mutant, allele A, have a mean that in mammals is produced by a gene on the sex- fitness wA, and the mean fitness of all individuals in the p determining Y chromosome. However, H-Y antigen is now population is wav (av average), then the increase in A’s known to be a result, not a cause, of the sexual phenotype frequency in the next generation due to selection if it has (Wolf 1998). Size dimorphism in vertebrates with GSD a starting frequency p is given by was not part of the evidence. Thus, the empirical evidence p(w Ϫ w ) to date has been very limited. A av .(1) The Kraak and de Looze (1993) model is based on the wav mechanistic idea that rate of embryonic growth determines gonadal differentiation (Mittwoch 1971), and it would pre- Clearly, factors that increase (1) will increase the mutant dict that ZW systems will tend to be characterized by allele’s resistance to random loss by genetic drift when rare higher female-to-male size dimorphism than XY systems (i.e., p is small). if embryonic growth rate reflects adult size. Thus, their In the case in which the allele is an ancestral sex- model focuses on the origin of a specific mechanism of determining allele, it is first easy to show that a dominant sex determination (alleles causing differential embryonic gene will be far better protected from random loss than growth) that might generate an association between sexual a recessive gene. This is important because it is possible size dimorphism and type of GSD system if the ancestral to develop an XY (or ZW) system through either the Y and W chromosomes increase growth rate (which is spread of a dominant male-producing gene on an incipient presumably favored by selection). The direction of the Y chromosome (or a dominant female-producing gene on an incipient W chromosome) or through the spread of a association that they predict is reversed, however, if the recessive female-producing gene on an incipient X chro- mutation reduces growth rate and reduced growth rate is mosome (or a recessive male-producing gene on an in- selectively favored. We consider patterns of selection that cipient Z chromosome). would generate the same association regardless of the pre- To show this, we assume that a male-producing gene cise mechanism and show that the association between on an incipient Y chromosome is dominant. In this case, GSD type and sexual dimorphism will be produced gen- w will be equal to f(x ϩ b) ϩ (1 Ϫ f)x, where f is the erally if body size tends to increase over the course of A probability that the allele is expressed in an individual that evolution, an assumption consistent with Cope’s rule would have become female in the absence of the gene’s (Kingsolver and Pfennig 2004). Thus, we show that the effect, x is the mean number of offspring produced by a association between sex chromosome system and sexual mating in the general population, and b is the additional dimorphism predicted by Kraak and de Looze (1993) is number of offspring produced by the mutant male. The even more general than implied by their model. mean fitness of all individuals in the population is virtually Below, we construct a simple mathematical model of equal to f(x) ϩ (1 Ϫ f)x p x. Expression (1) thus becomes the evolutionary origin of GSD systems from ESD. In par- equal to pfb/x for the dominant allele. The case of a re- ticular, we adopt the perspective from protected invasion cessive female-causing allele is quite different. In this case, theory (Reeve 1993; Reeve and Shellman-Reeve 1997) that the allele has a selective advantage only when expressed a favored genetic variant that is especially likely to survive in a male and when this male has an A allele at the ho- random loss through genetic drift when rare is most likely p Ϫ ϩ ϩ Ϫ mologous locus, yielding wA p(1 f)(x b) (1 to be responsible for the origin of its associated novel p)(1 Ϫ f)(x) ϩ fx. In this case, (1) becomes equal to phenotype. For example, if two different variants con- p2(1 Ϫ f)b/x, which is much smaller than the expression ceivably could confer fitness advantages, then the one with for the dominant allele for small p. Thus, we can conclude the stronger selective advantage when rare will be especially that there should be, from protected invasion theory, a likely to result in the origin of a novel trait, creating an strong bias toward origin of XY systems from the spread origin bias that will be detectable phylogenetically. We of dominant Y alleles over the spread of recessive X alleles. show that the resulting model predicts a strong relation- Parallel logic leads us to restrict our attention to dominant ship between sexual size dimorphism and GSD system and W alleles in the origin of ZW systems. A focus of dominant 522 The American Naturalist alleles is also consistent with the consensus in the literature respond independently to the environmental stimuli, with on the genetics of sex determination (Bachtrog et al. 2011). the mutant A allele inducing the sexual characteristics Once we restrict our focus to dominant alleles, we can without necessarily inducing the larger body size. The mu- now turn our attention to origin biases that result from tant A-containing males are thus larger on average than different patterns of selection on male and female body wild-type males, and since selection favors larger males, size. We have to take into account the statistical tendency the A allele spreads, generating a primordial Y chromo- for lineages to increase rather than decrease in body size some. After spread of the allele to some intermediate fre- over evolutionary time, which appears to be driven in quency, selection on modifier loci would be expected to vertebrate taxa by consistent within-population selection genetically couple the body size increase to the sex change for larger body size (Kingsolver and Pfennig 2004). Such induced by the A allele. consistent selection for larger body size would be expected In the last combination, males are initially larger than from coevolutionary size races between predators and prey females, the A allele causes a male to develop into a large or between conspecific or heterospecific competitors. female instead of a large male, and selection favors an Given that, on average, selection in an evolving popu- increase in the relative size of females. The mutant A- lation will tend to favor larger males or females, it is pos- containing females are thus larger on average than wild- sible to examine associations between type of GSD system type females, and since selection favors larger females, the and sexual dimorphism that would be predicted by pro- A allele spreads, generating a primordial W chromosome. tected invasion theory. We must consider the outcomes of After spread of the allele to some intermediate frequency, selection on a dominant A allele that causes bigger males selection on modifier loci would be expected to genetically or females for all possible conditions of ancestral size di- couple the size increase to the sex change induced by the morphism and for both the case that selection favors bigger A allele. males and the case that selection favors bigger females. We In the combination in the second row, an A allele causes show the latter combinations and their associated out- an individual that otherwise would have been a female to comes in table 1. become male, and such a male, because it is smaller than In the first combination, females are initially larger than the average ESD-produced male, will have reduced fitness males, the A allele causes a female to develop into a large (A is disfavored). By a similar logic, in all of the other male instead of a large female, and selection favors an remaining combinations, the mutant allele is either neutral increase in the relative size of males (table 1). Note that or selectively disfavored and thus obviously highly vul- in this theory, in contrast to that of Kraak and de Looze nerable to loss. (1993), we are assuming that the mutant allele changes This model for biases in the origin of GSD with respect the sexual characteristics but the body size can still be set to sexual dimorphism does not require that the dimor- by the local environmental stimuli (e.g., temperature). In phism is reversed. It is sufficient that the dimorphism is other words, size and sexual characteristics in ESD might reduced, with the sex produced by the dominant sex allele

Table 1: Different outcomes of selection on rare, dominant A alleles producing males (M) or females (F) for different combinations of ancestral dimorphism in an environmental sex determination (ESD) system and for different patterns of new sex-specific selection pressures Ancestral dimorphism Dominant A Selection favors in ESD system allele produces bigger Outcome F 1 M Males Males A favored; XY system origin; M increase in size relative to F F ! M Males Males A disfavored F 1 M Males Females A disfavored F ! M Males Females A disfavored F 1 M Females Males A disfavored F ! M Females Males A disfavored F 1 M Females Females A disfavored F ! M Females Females A favored; ZW system origin; F increase in size relative to M Note: For ancestral sexual dimorphism states and sex-specific selection patterns, we consider only strict inequalities for simplicity, without lossof generality, since exact equality is likely rare. “Selection favors bigger males” means new selection pressures (possibly different from the ancestral ones, due to changed environments) favor relatively large males and relatively small females; “Selection favors bigger females” means the reverse. “A disfavored” refers to cases in which the A allele causes reduced fitness. For example, in the case described by the second row, an A allele causes an individual that otherwise would have been a female to become male, and such a male, because it is smaller than the average ESD-produced male, will have reduced fitness. Origin of Sex-Determination Systems 523 becoming closer to the opposite sex in size (table 1). This differentiate between those two possibilities, only one of is because this dominant allele spreads when selection which is consistent with the model? starts favoring an increase in the size of a sex that is initially One possible way around this causal ambiguity would smaller than the opposite sex. One way to achieve this is be to compare sex-conditioned phenotypes between sister via the mutant switching the sex of an individual destined taxa that possess versus lack GSD. For example, if male to become the bigger sex under the old ancestral ESD rule. size increase predisposed an XY system, then lineages that The dominant mutant spreads even if the mutant indi- exhibit an XY system as a newly derived state should ex- vidual is not bigger than the bigger sex of the old ESD hibit larger males along with sister taxa lacking the XY rule, because it is bigger than the sex it would have been system (the latter taxa exhibiting the plesiomorphic state under that rule. of ESD). In contrast, if larger males resulted from an XY The only two GSD origins permitted in table 1 thus system, then neither larger males nor an XY system should predict that there should be a statistical association be- be exhibited by the sister taxa, suggesting that larger males tween sexual dimorphism and type of GSD. In particular, evolved after the establishment of the XY system. No re- transitions to XY systems should tend to be accompanied lationship between sexual size dimorphism and kind of by increases in the size of males relative to females, and GSD would invalidate the protected invasion hypothesis. transitions to ZW systems should tend to be accompanied A test of that kind would require resolved phylogenies that by increases in the size of females relative to males. This do not yet exist. is the central prediction that we sought to test. An alternative approach to resolving the causal ambi- guity is to see whether the hypothesized predisposing phe- notype is associated with GSD type in clades where GSD XY and ZW GSD Systems as Causes versus ancestry is likely. If body size dimorphism is causal, then Consequences of Sex-Specific Phenotypes the association should be found only where an ESD an- cestry is possible. If it is a consequence, then it should be Once incipient XY and ZW systems are established, sub- found regardless of ESD versus GSD ancestry. Therefore, sequent selection is predicted by several recent models to in testing the model, we will begin with a test of the central reduce the rates of recombination between chromosomes prediction for ESD ancestry, where body size dimorphism containing the sex-determining genetic locus (Charles- is causal, and then in a second test ask whether the same worth 1991; Rice 1994), leading eventually to the emer- association is found when there is unlikely to be ESD gence of true, that is, nonrecombining, sex chromosomes. ancestry. As the sex chromosomes become more strongly differ- entiated, protected invasion effects will become increas- ingly potent in causing phenotypic divergence between the Testing the Model with Comparative sexes. In particular, the homogametic sex will be especially Evidence from Vertebrates likely to move from a previously sexually monomorphic Prediction: XY Systems Will Be Associated with a phenotypic optimum to a new, sex-conditional phenotypic Relatively Larger Ratio of Male to Female optimum such as that associated with parental or allo- Body Size than ZW Systems parental care (Reeve and Shellman-Reeve 1997) or elab- orated gametic investment such as exhibited in viviparity. Testing this prediction requires an analysis that asks This creates a potential problem for testing our model. whether there is a statistically significant association be- The new sex-conditional phenotypic optimum might in- tween the two characters (GSD type and sexual size di- volve the very same phenotypic attributes that were earlier morphism) independent of shared phylogeny. Methods for identified as predisposing the origination of XY or ZW such a test are usually designed to address a problem of sex-determination systems. For example, increases in the nonindependence of data points, require branch lengths size of males relative to females were earlier shown to for the underlying phylogeny, or assume continuous, predispose the origination of XY systems from an ancestral rather than categorical, character variables. For our data state of ESD, but larger males might also arise as a con- set, however, some of the different pairs of taxa come from sequence of the establishment of a differentiated XY ge- different regions of vertebrate phylogeny (different fami- netic system. This ambiguity in the direction of the causal lies, orders, and classes) and include many regions with arrow raises a problem for empirical tests of our predic- unresolved phylogenies. Each pair diverged a very long tions about the conditions favoring alternative GSD sys- time ago from every other pair. Given how labile sex de- tems: Did the sex-limited phenotypes associated with dif- termination and body size dimorphism appear to be, and ferent genetic systems cause or result from those systems how many separate origins there have been, the pairs and via protected invasion effects? What kinds of tests could their GSD and size-dimorphism states can safely be as- 524 The American Naturalist sumed to have arisen independently rather than through about body size dimorphism could be found for one or shared phylogeny. Nor are accurate branch lengths possible both of the pair members. These pairs could not be in- across our data set. Furthermore, GSD type is a two-cat- cluded in the analysis. egory discrete-valued character. Therefore, the analysis was Size-dimorphism states are based on adult body length carried out by using a simple nonparametric test, the sign (standard length for teleosts, carapace length for turtles, test, to see whether matched pairs of taxa differing in GSD snout-vent length for lizards). Mean sizes of adult males type differed in size dimorphism in the predicted direction and females were located whenever possible and used to (Felsenstein 1985; Møller and Birkhead 1992; Stockley et determine the sexual size dimorphism (SSD) index rec- al. 1997). This simple method is statistically conservative ommended by Lovich and Gibbons (1992) and used (has low power) and has the advantage that it makes no throughout Fairbairn et al. (2007). SSD is calculated as assumptions about the underlying phylogeny. (larger sex/smaller sex) Ϫ 1 and is made negative if males This method was applied to the three vertebrate groups are larger and positive if females are larger. Thus, no size that (a) contain both GSD types and (b) are most likely difference equals 0, and SSD is symmetrical around 0. to be derived from an ESD ancestral state: the Teleostei, Where multiple reports gave different means or SSDs for Chelonia, and (within the Sauria) Gekkota. With respect the same species, the mean SSD was used. Where a set of to teleosts, some form of ESD has been found in most multiple species was the match, the mean SSD for the set families that have been studied and in at least 11 orders, was used in the analysis. In a few cases, only size ranges including the somewhat basal Anguilliformes, and new and or maximum sizes could be found and were used instead taxonomically widespread reports of ESD are increasing of means. (Devlin and Nagahama 2002; Valenzuela and Lance 2004). The results are shown in table 2. There are 16 matched Forms of ESD in which environment interacts with genes pairs of species that differ in GSD type for which size to determine sex are very common and also taxonomically dimorphism information could be located. Of these 16 widespread (Baroiller and D’Cotta 2001; Valenzuela et al. pairs, 14 differ in SSD in the predicted direction, with 2003). Pairs were formed with species in clades where ESD lower SSDs (relatively larger males) in the XY species (two- is also present. Species with known GSD of different types tailed P p .004). (Recall that, as explained earlier, com- were regarded as forming pairs if they were in the same plete reversal of size dimorphism is neither predicted nor family or (if there were no other family members with required under the model.) Even minus the two pairs known GSD type or no within-family type diversity) the (pairs 11 and 12) where SSDs based on means have to be same order. Some lizard groups also contain mixtures of compared with SSDs based on maxima, which might bias genetic and temperature sex determination (Valenzuela et the outcome, the predicted result is still statistically sig- al. 2003; Sarre et al. 2004; Organ and Janes 2008), and an nificant (P p .013). ESD ancestry has been proposed for squamates generally and the Gekkota in particular (Janzen and Paukstis 1991; Generality of the Association between GSD Type Donnellan et al. 1999; Pokorna and Kratochvı´l 2009; but and Body Size Dimorphism see Janzen and Phillips 2006). Among turtles, most species that have been studied have TSD, and the phylogenetic The model predicted this association for species with an position of those with GSD supports the evolution of GSD ESD ancestry. The association would not be predicted to from ESD (Janzen and Paukstis 1991). extend to vertebrates representing transitions from one Information about GSD type was obtained from reviews GSD type to the other. It is possible to do the same kind (Hillis and Green 1990; Janzen and Paukstis 1991; Klink- of analysis as in table 2 using only comparisons likely to hardt et al. 1995; Schmid and Steinlein 2001; Devlin and have GSD ancestry. One group of species suitable for such Nagahama 2002) and by using Web of Science (ISI Web an analysis consists of amphibians. It has been well es- of Knowledge, Thomson Scientific, last search February tablished that all amphibians have GSD, and ancestral re- 2011). GSD types were assigned to two categories, XY and construction strongly supports GSD ancestry (Hillis and ZW. The XY (XX/XY) category includes multiple sex chro- Green 1990; Hayes 1998). Another group consists of mosome systems (e.g., XXXX/XXXY), and ZW (ZZ/ZW) closely related pairs of fish species that are discussed in includes analogous variants. Information about the adult the sex-determination literature as representing transitions sexual size dimorphism of those species with known GSD from one GSD type to another. The results for these two type was then obtained by using Web of Science (ISI Web groups are shown in table 3. In this analysis of species of Knowledge, Thomson Scientific, last search February with confirmed or likely GSD ancestry, containing 13 com- 2013) and a Google (http://www.google.com/) web search parisons (6 for teleosts and 7 for amphibians), there was (to locate journal articles missed by the Web of Science no statistically significant association in the predicted di- search function). For some matched pairs, no information rection between GSD type and sexual size dimorphism Origin of Sex-Determination Systems 525

(P p .092). Only four pairs were consistent with the pre- against this possibility is that the association was only sta- diction, and instead more than half the pairs differed in tistically significant for animals that might have had an the opposite direction. This further suggests that the as- ESD ancestry. Another is that sex differences in body size sociation in table 2 is related to the evolution of GSD from are not highly correlated with intersexual selection (e.g., ESD and not some other property of the two GSD types. with the extreme male traits that females prefer; Fairbairn et al. 2007). Degree and direction of body size dimorphism are a result of multiple selective forces, some acting on General Discussion absolute sizes of males, others acting on absolute sizes of To our knowledge, this is the first attempt to understand females, and yet others whose fitness consequences will the phylogenetic distribution of vertebrate genetic sex- depend on the relative sizes of the two sexes. Intrasexual determining systems by using a formal model to generate selection is often more important than intersexual selec- predictions that are then tested empirically using a com- tion (Shine 1979, 1989; Reeve and Fairbairn 2001; Monnet parative statistical method. Support for the model for the and Cherry 2002). “Fancy” males aren’t necessarily larger evolution of GSD from ESD came from the analysis of than the females choosing them. Sexual selection produces sexual size dimorphism. GSD type was associated with smaller as well as larger males, as in guppies where males body size dimorphism independently of shared phylogeny, are small but colorful. Larger size may benefit males that such that in pairs of related taxa, those with an XY system engage in combat, but larger size may benefit female fe- had relatively larger males (compared to females) than cundity even more. Once a GSD type has evolved from those with a ZW system. Furthermore, this association was ESD and sex chromosomes have become heteromorphic, only statistically significant for pairs that could have some however, the sex chromosome architecture could affect the ESD ancestry. The prediction of an association between likelihood that intersexual selection could alter any pre- GSD type and sexual size dimorphism in the evolution of existing size dimorphism. This would also be the case when GSD from ESD was first presented by Kraak and de Looze a GSD type has evolved from another GSD type. In table (1993). We show that the prediction is more general than 3, more than half the pairs differed in the opposite direc- implied by their specific mechanistic explanation for the tion from the prediction for the evolution of GSD from evolution of GSD from TSD. ESD. As more size dimorphism information becomes Body size dimorphism in the model is not a determinant available, it will be possible to see whether this association of GSD type or an invariable predictor that a particular (which is not currently statistically significant) continues type will evolve. Rather, it is one of several factors that and whether it reflects a causal influence of sex chro- could tip the balance to enable a mutation for a new GSD mosome architecture on the evolution of sexual size type to spread instead of become extinct. Also, a change dimorphism. in body size dimorphism is not sufficient for a change in The model traces the evolution of GSD via a dominant GSD type, for example, if the sex chromosomes have be- allele or alleles acting in the heterogametic sex. Among come highly heteromorphic (gone to fixation). Thus, body vertebrates, there are only a few species, most of them size dimorphism is neither necessary nor sufficient, al- mammals, for which there is sufficient evidence to tell though it may be strongly predisposing. whether GSD is produced by a dominant allele as opposed In the model, XY or ZW systems are consequences of to a balance between several alleles. In mammals, evidence selection for larger male or female body size, not neces- points to a dominant testis-determining gene (Sry) on the sarily causes of the evolution of body size dimorphism. Y chromosome (Mittwoch 1996; Vaiman and Pailhoux One way that the sex-determining system could cause body 2000). In the African clawed frog Xenopus laevis,aZW size dimorphism is if body size is sex linked. Some ver- species, there appears to be a dominant female-determin- tebrates such as poeciliid fishes have sex-linked body size ing gene (Yoshimoto and Ito 2011). A male sex-deter- (Roldan and Gomendio 1999; Lindholm and Breden mining gene (DMY) analogous to the mammalian Sry was 2002). Pleiotropy or sex linkage does not seem to account identified in the teleost Oryzias latipes, but it appears that for GSD vertebrates generally, however, because the as- a similar role for DMY does not generalize to other teleosts sociation between which sex is heterogametic and which (Matsuda 2005; Takehana et al. 2007; Tanaka et al. 2007). is larger is far from perfect. Nonetheless, once male or Interestingly, two other Oryzias species (O. hubbsi and O. female heterogamety with heteromorphic sex chromo- javanicus) do not have the same type of sex determination somes has evolved, the two GSD types have different con- as O. latipes but instead have ZW systems (Takehana et sequences for the evolution of extreme male traits under al. 2007). No size dimorphism information appears to be female choice (Reeve and Pfennig 2003). Could this have available for those ZW species to enable adding this com- produced the association in table 2 rather than the direc- parison to table 3 (GSD-to-GSD transitions). Nonetheless, tion of causation posited by the model? One argument medakas have excellent potential for illuminating the se- 4 3 9 2 8 7 5 6 12 10 11 13 16 14 15 Sources a ZW Ϫ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ Ϫ ϩ ϩ ϩ ϩ ! XY for this pair? (weight) .05 .18? .02 .11 .02 .21 .01 .22 .12 .17 .85.50 1 .48 .31 .22 .34 .63 .15 .08 .16 .36 1.1 Ϫ Ϫ Ϫ Mean Mean Loricariichthys platymetopon Cynoglossus puncticeps Boleophthalmus boddaerti Colisa fasciata Triportheus guentheri Eleotris pisonis Scardinius erythrophthalmus Leuciscus pyrenaicus Apeltes quadracus Anguilla anguilla Anguilla rostrata Gambusia nobilis Gambusia hurtadoi Gambusia puncticulata Heterobranchus longifilis Pleuronectes platessus Gekko hokouensis Esox masquinongy Scophthalmus maximus Kachuga smithii ,.06 .08 .02 .10 .21 .01 .47 .03 .05 .09 .18 .06 .46 .28 .07 .30 .03 .04–.10 .17 .02 .09 Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Mean Mean (7 spp.) Hypostomus ancistroides Gobionellus shufeldti Betta splendens Symphurus plagiusa Hoplias malabaricus Dormitator maculatus Cyprinus carpio Vimba vimba Carassius auratus Pungitius pungitius Gymnothorax eurostus Limia perugiae Heteropneustes fossilis Oncorhynchus Pseudopleuronectes yokohamae Bothus podas Gekko japonicus Siebenrockiella crassicollis c b e d f Independent paired comparisons test of the model: sexual size dimorphism (SSD) of matched pairs differing in genetic sex determination (GSD) type 5 Clariidae/Heteropneustidae 4 Loricariidae 3 Characiformes 9 Eleotridae 2 Cyprinidae 8 Gasterosteidae 1 Anguilliformes 6 Salmoniformes/Esociformes 7 Poeciliidae 13 Pleuronectidae 1011 Gobiidae 12 Osphronemidae Cynoglossidae 14 Scophthalmidae/Bothidae 15 Bataguridae 16 Gekkonidae Table 2: PairTeleost fishes: Order or family Species with XX/XY GSD SSD Species with ZZ/ZW GSD SSD Turtles: Geckos:

526 , ,F 360, GSD GSD 126); ϩ ϩ p p , F mean , F mean Leuciscus Apeltes GSD types: , F mean 22, p , F mean 178, M 45–190). mean lengths for Cyprinus Scardinius ϩ 157); Cal et al. 2006 128, M mean 129). 6 GSD types: Devlin and ϩ ϩ G. hurtadoi , 7 spp., SSDs based on ¨sler et al. (2011). ϩ p n maximum lengths are in , F mean 239, M mean 244); , F mean parison, the species mean SSD is Pseudopleuronectes ( , F 28–95, M 28–105). 12 a logeny of Ro 134, M mean Oncorhynchus 210, M mean ϩ Colisa ϩ 181, F 45–202, M mean Triportheus Boleophthalmus ϩ , F mean 132); Geraldes and Collares-Pereira 1995 ( , F mean GSD types: Kavumpurath and Pandian 1994; Devlin ϩ , F 237–407, M 283–595, males significantly larger). 2 , F mean p Bothus , F mean 58, M mean 57). 960); Young 2005 ( 390); Lee et al. 2009 GSD types: Moritz 1990; Kawai et al. 2009; Gamble 2010. s genus. Based on phy , multiple sites, SSDs 0.31–0.48, mean SSD 0.39); Swenton ϩ ϩ GSD types: Ross et al. 2009. Sizes: Rowland 1974 ( p 0.10). 11 p Symphurus , F mean 243, M mean 256); Fatemi et al. 2009 ( Heterobranchus 172, M mean Ϫ Gymnothorax , two sites, F means 229 and 207, M means 203 and 201, SSDs 0.13 G. japonicus ϩ 450, M mean , no significant size dimorphism reported but no data provided); Nordlie G. puncticulata 1090, M mean Scardinius ϩ , F mean ϩ Hypostomus GSD types: Carr and Bickham 1981; Janzen and Paukstis 1991. Sizes: Honegger GSD types: Devlin and Nagahama 2002; Oliveira and Toledo 2006. Sizes: Perrone Eleotris 0.19, mean SSD p 247, 234, 270, SSDs 0.27, 0.40, 0.37, mean SSD 0.35). 14 p sex determination in thi Ϫ , F 520–890, M 300–480, no overlap in the size distributions); Oliveira and McCleave , F mean ϩ Leuciscus , F mean , no lengths reported, F mean weight 2.7 kg, M mean weight 2.4 kg); Nash et al. 1991 ´c et al. 2001 ( Esox 0.06). 9 , F 153–227, M 101–108). 16 163 and 200, SSDs 0.26 and 0.10, mean SSD 0.18); Emiroglu et al. 2010 ( p A. anguilla ϩ Pleuronectes ´c Popovı Kachuga Scophthalmus , F 20–60, M 20–70, mean for the oldest age group, are as follows. Where no means could be located, length ranges are given. GSD types: Devlin and Nagahama 2002. Sizes: Godinho 1997 ( p 149); Topı , F mean 176, M mean 165); Baras 1999 ( p 314, 327, 370, M means ϩ ϩ GSD types: Angus 1989; Devlin and Nagahama 2002. Sizes: Hubbs and Springer 1957 ( ϩ Dormitator p 0.02–0.17, mean SSD 171). 3 , F mean 64, M mean 59); Jono and Inui 2012 ( , F mean 24, F maximum ?, M mean 29, M maximum 36); Paswan 2012 ( , multiple sites, SSDs 0.13–0.30, mean SSD 0.23). 8 Ϫ 206 and 219, M means ϩ ´ndez-Delgado and Herrera 1995 ( male, mean Betta ϩ 3, F 112 and 146, M 109); Terwilliger and Munroe 1999 ( Heteropneustes 1040). 7 181, M mean , three sites, F means 221, 202, and 208, M means 211, 188, and 204, SSDs 0.05, 0.07, and 0.02, mean SSD 0.05). 5 p p ϩ ϩ table 2 because there is also environmental N , G. hokouensis G. puncticulata GSD types: Pezold 1984; Devlin and Nagahama 2002. Sizes: Clayton and Vaughan 1982 ( 179, M mean GSD types: Alves et al. 2006. Sizes: Viana et al. 2008 ( female, M ϩ p , F mean p Loricariichthys p Cynoglossus , 11 populations, SSDs 1230, M mean , three year periods, F means ϩ Leuciscus , F mean ´ez et al. 2012 ( , two populations, F means Pungitius Vimba no. , F mean p , F mean 67, M mean 64, , two populations, F means 39 and 43, M means 39 and 51, SSDs 0 and Esox , five populations, SSDs 0.04–0.39, mean SSD 0.28); Abney and Rakocinski 2004 ( Carassius Pseudopleuronectes ( b Limia on is between congeners, it belongs in 164); Pires et al. 2000 ( , F mean 240, M mean 242). 4 GSD types: Devlin and Nagahama 2002. Sizes: de Leo and Gatto 1995 ( Gobionellus G. japonicus , F 15–90, M 15–109); Winemiller and Ponwith 1998 ( ϩ p , F mean 158, M mean 145, size distributions overlapped); Moll 1987 ( yes; a minus sign ¨der 1996 ( Hoplias Eleotris , F maximum 71, M maximum 125). 10 , F mean 521, M mean 347, a 400-mm cutoff distinguished the sexes with 99.7% accuracy); Loh et al. 2011 ( p , F mean 31, M mean 21); Pa .004, sign test (0.013 without pairs 11 and 12). See text for method used to form comparisons and formula for SSD. SSDs are based on adult mean lengths, or , no lengths reported, F eviscerated mean weight 3.5 kg, M eviscerated mean weight 2.2 kg). 15 p 290); Lee et al. 2009 191, M mean P ϩ ϩ , F 115–160, M 85–190, most of the larger individuals caught were males, no length-weight sex difference); Schintu et al. 1994 ( GSD types: Felip et al. 2001; Luckenbach et al. 2009. Sizes: Rijnsdorp and Ibelings 1989 ( G. nobilis Siebenrockiella A. rostrata Dormitator Based on phylogeny of Roje (2010). Related genera of siluriform catfishes, according to Diogo et al. (2003). A plus sign Sister groups in the Mank et al. (2005)Based teleost on supertree. phylogeny of Azevedo et al. (2008). Although this comparis p GSD types: Bongers et al. 1999; Devlin and Nagahama 2002. Sizes: Ferna Sources: Source citations and body lengths, where F a b c d e f Note: Bothus Scophthalmus Pezold and Gilbert 1987 ( 2000 ( and Nagahama 2002. Sizes: Jaroensutasinee and Jaroensutasinee 2001 ( 13 mean 42, M mean 36); Herczeg et al. 2010 ( M mean and Vieira 1990 ( types: Luckenbach et al. 2009. Sizes: Seshappa 1976 ( M mean 18); Schro 2011 ( 226, M mean 213); Okgerman et al. 2011 ( Prado et al. 2006 ( types: Teugels et al. 1992; Christopher et al. 2010. Sizes: Bhatt 1968 ( and 0.03, mean SSD 0.08); Garcia and Benedito 2010 ( F mean 2000 ( p All lengths are mm. 1 Nagahama 2002; Haffray et( al. 2009; Martinez et al. 2009. Sizes: Devauchelle et al. 1988 ( mean body sizes); Casselman 2007 ( 355, M mean 346); Patimar 2009 ( Dabrowski et al. 2000; Devlin and Nagahama 2002; Phillips 2007. Sizes: Harrison and Hadley 1979 ( 1986 ( ( Sizes: Zhang et al. 2009 ( the oldest age categories,regular when type. possible Where and there on are maximum multiple lengths sources for only a when species, no the means mean can of be the located. SSDs SSDs is based given. on Where means there are are shown multiple in species in boldface; the SSDs XY based or o ZW half of the com compared.

527 tched 9 7 6 4 1 3 2 10 12 13 Sources a ZW p / Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ ϩ Ϫ ϩ ϩ Ϫ Ϫ ! Ϫ XY for this pair? .06 5 Ϫ (weight) ,.31 , ,.65 .00 .44.25 11 .13 .05 .21 .09 8 .18 .03 .08 .03 .22 .08 .15 .07 .33 .47 .30 .28 .23 .11 .17 Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Mean .38 Mean Mean Mean Mean c b Eleutherodactylus euphronides Eleutherodactylus johnstonei Discoglossus pictus Buergeria buergeri Hoplobatrachus tigerinus Siren intermedia Aneides ferreus Pleurodeles waltl Tilapia mariae Clarias batrachus Oreochromis aureus Oreochromis karongae Bufo bufo Bufo marinus Xiphophorus helleri Gambusia affinis Poecilia sphenops Poecilia latipinna .01 Ϫ .30 .17 (weight) ,.57 – – , ,.67 .60 .05 .05 .02 .07 .01 .05 .13 .09 .12 .10 .08 .24 .07 .03 .35 .22 .26 Ϫ Ϫ Ϫ Ϫ Ϫ Mean Mean Mean (7 spp.) (12 spp.) ed by the model to show a significant association Eleutherodactylus riveroi Rana Bombina orientalis Triturus Necturus maculosus Necturus alabamensis Necturus beyeri Hydromantes ambrosii Tilapia zillii Clarias fuscus Oreochromis niloticus Bufo viridis Gambusia holbrooki Xiphophorus andersi Poecilia reticulata Independent comparisons test of the generality of the association between genetic sex determination (GSD) type and sexual size dimorphism (SSD): ma 8 Salamandridae 7 Proteidae/Sirenidae 9 Plethodontidae 6 Cichlidae 1 Clariidae 5 Cichlidae 2 Poeciliidae 4 Poeciliidae 3 Poeciliidae 11 Leptodactylidae 12 Ranidae/Mantellidae/Rhacophoridae 10 Bombinatoridae/Alytidae 13 Bufonidae Amphibians: pairs differing in GSD type that are not predict Table 3: PairTeleost fishes: Family Species with XX/XY GSD SSD Species with ZZ/ZW GSD SSD

528 , E. N. ´n- 0.14, Rana Ϫ , 14 sites, 0.09–0.15, , lists male GSD types: Ϫ p Rana japonica , 0.22 and Ϫ X. helleri , F 86–257, M 65– Pleurodeles Rana blairi , SSD 0.17); Malmgren and O. niloticus , two populations, F means 50, , mean SSD 0.02); AmphibiaWeb Where there are multiple sources ection from that predicted by the GSD types: Devlin and Nagahama , F maximum 40, M 17–29); Bisazza p , F mean 162, M mean 173); Beltra within the Plethodontidae. SSDs and Triturus boscai T. vulgaris Discoglossus amily variation in GSD type), the phylogeny e direction as the pairs in table 2, because the G. holbrooki O. niloticus , F mean 122, M mean 113); Monnet and Cherry , F mean 32, M mean 24); Ortega et al. 2005 ( , F mean 287, M mean 348); Moreno et al. 2006 ( , two populations, F means 79, 69, M means 77, 66, SSDs Siren B. marinus , mean SSD 0.14, , SSDs 0.08, 0.07, 0.30, and 0.16, respectively); Gramapurohit , F 15–43, M 14–26). 3 E. johnstonei GSD types: Hillis and Green 1990. Sizes: Woolbright 1983 ( B. viridis rmation could be found. p G. affinis GSD types: Schmid et al. 2002; Schmid et al. 2003. Sizes: Ovaska 1992 , F monthly means 54–65, M monthly means 49–63, SSDs p , no length reported, F mean weight 246 g, M mean weight 306 g); Srivastava Triturus helveticus Aneides Rana nigromaculata , two sites, F means 222 and 213, M means 271 and 243, SSDs m information could be found. , F maximum 55, M maximum 45); Basolo and Wagner 2004 ( , SSD 0.15); Caetano and Leclair 1999 ( , SSDs 0.16 and 0.07, respectively); AmphibiaWeb 2013 ( , and C. fuscus , F 105–370, M 100–403, no significant difference between the sexes). 6 size dimorphism info T. mariae ¨ck et al. 2011. Sizes: Lee 2001 ( GSD types: King 1990; Schmid and Steinlein 2001. Sizes: Shine 1979 ( X. andersi p , mean SSD 0.17, O. aureus , two populations, F means 67, 50, M means 43, 37, SSDs, 0.56, 0.35, mean SSD 0.47); Khonsue Rana rugosa Triturus italicus Rana ridibunda , and , F mean 43, M mean 41). 11 , F 127–180, M 130–192); Frese et al. 2003 ( T. alpestris Buergeria GSD types: Black and Howell 1979. Sizes: McPeek 1992 ( , F 17–63, M 13–32); Deaton 2008 ( , F maximum 39, M maximum 27). 12 GSD types: Hillis and Green 1990. Sizes: Capula and Corti 1993 ( p , SSD 0.11, p Bombina , F mean 64, M mean 63); Kutrup et al. 2011 ( Rana temporaria , yer (1997) for which size dimorphis N. maculosus Rana esculenta G. holbrooki ¨l et al. 2009 ( E. euphronides B. viridis male, are as follows. Where no means could be located, length ranges or maximum lengths are given. All lengths are mm. 1 , F mean 32, F 30–36, M mean 20, M 16–23); Bourne 1997 ( Triturus carnifex , F mean 335, M mean 306). 8 GSD types: Abramyan et al. 2009; Sto p p Rana catesbeiana phylogeny of Me E. riveroi N. beyeri , F mean 76, M mean 82); Russell et al. 2012 ( , SSD 0.08); Ueda et al. 1998 ( GSD types: Hillis and Green 1990. Sizes: McKenzie 1969 ( , SSD 0.03); Denoe , SSD 0.16, female, M p p T. zillii , F mean 66, M mean 60). 10 ding to the phylogeny of Pouyaud et al. (2009) for which Rana pipiens , F maximum 300, M maximum 290, but more males than females were large); Nguyen et al. 2007 ( GSD types: Baroiller et al. 1995; Devlin and Nagahama 2002; Lee et al. 2004; Cnaani et al. 2008. Sizes: Abubakar 1997 ( Triturus vulgaris p Triturus alpestris H. ambrosii no. ngener according to the , SSD 0.35); Vargas and de Sostoa 1996 ( p O. karongae 0.07). 5 Ϫ , SSD 0.06, GSD types: Kallman 1984; Volff and Schartl 2001. Sizes: Wischnath 1993 ( 0.05, 0.13, and 0.29, respectively). 13 , F mean 208, F 125–307, M mean 225, M 131–315); Messina et al. 2010 ( 0.04 and 0.04, mean SSD 0.00); Zeyl and Laberge 2011 ( Ϫ p G. holbrooki Ϫ , F mean 153, M mean 135); Tryjanowski et al. 2006 ( , SSD 0.18); Monnet and Cherry 2002 ( GSD types: Hillis and Green 1990. Sizes: Shoop 1965 ( , SSDs p O. aureus yes; a minus sign , no length reported, F mean weight 160 g, M mean weight 120 g). 2 Triturus cristatus , F maximum 286, M maximum 312). 9 p , SSD 0.28, .092, sign test (.146 if pair 5, where the SSDs are very close, is indicated with an equal sign). More than half the comparisons differ in the opposite dir 0.27–0.8, mean SSD , F 21–38, M 20–25); Lynch and La Marca 1993 ( 0.18). 7 , six sites, SSDs 0.19–0.26, mean SSD 0.22); Sinsch et al. 2007 ( Ϫ Hoplobatrachus Rana brevipoda , F mean 170, M mean 169); McDaniel et al. 2009 ( Ϫ p , F mean 27, F 23–32, M mean 23, M 17–29); AmphibiaWeb 2013 ( , SSD 0.07); Yekta and Blackburn 1992 ( P C. batrachus G. affinis Pleurodeles B. bufo Rana tsushimensis The most closely related ZZ/ZW congener accor A plus sign The most closely related ZZ/ZW co GSD types: Pandey and Lakra 1997; Galbusera et al. 2000; Devlin and Nagahama 2002. Sizes: Qin et al. 1998 ( Note: a b c Sources: Source citations and body lengths, where F lvarez et al. 2010 ( E. johnstonei ´ in Frost et al.comparisons between (2006) SSDs was are used based on to means determine when the possible and most on closely maximum related lengths when family no with means can a be different located. GSD SSDs based type. on This means are phylogeny shown was in also boldface. used to determine the pair johnstonei model for species with environmentalGSD types sex are determination unlikely (ESD) to ancestry. have The evolved table from contains ESD. comparisons Where that amphibians needed would to not be be paired expected with to members differ of in different the families sam (because there was no within-f 2012 ( 1993 ( 0.03, 0.05). ( clamitans et al. 2002 ( et al. 2004 ( 2013 ( mean SSD 0.05); Salvidio51, and M Bruce means 2006 52, ( 49, SSDs 2002 Sizes: Bisazza 1993. 4 p and for a species, the mean of the SSDs is given. Where there are multiple species in the XY or ZW half of the comparison, the species mean SSD is compared. SSDs range 2002 ( 260); Msiska and Costa-Pierce 1999 ( alabamensis A as the larger sex);Thollesson Joly 1999 and ( Giacoma 1992 ( Cnaani et al. 2008. Sizes:mean Ishikawa SSD and Tachihara 2008 (

529 530 The American Naturalist lective pressures and molecular mechanisms for transitions sexual selection can produce (Roldan and Gomendio 1999; from one GSD type to another, as do the Lake Malawi Kirkpatrick and Hall 2004) and introduces a major bias cichlids of the genus Metriaclima, which appear to have in which sex will evolve a novel extreme trait such as quite diverse and evolutionarily labile genetic sex-deter- cooperative breeding or “fancy” ornaments (Reeve and mining systems (Ser et al. 2010). Pfennig 2003). The possibility of important consequences Models for the evolution of GSD types from simulta- for developmental processes such as sexual differentiation neous hermaphroditism can also be developed, but most has been recognized for some time but remains to be animal genetic sex-determining systems probably did not explored formally and statistically (Witschi 1959; Jost 1960; evolve from simultaneous hermaphroditism (Bull 1983; Mittwoch 1975; Adkins-Regan 1981). Charlesworth and Mank 2010). Living members of basal vertebrate lineages are not hermaphroditic. Instead, the most common form of hermaphroditism in vertebrates, which occurs in some perciform teleost Acknowledgments fishes, is successive hermaphroditism, a form of ESD. Most We thank I. Lovette for expert advice about the compar- cases appear to be derived from GSD rather than ancestral ative statistical approach and J. Bull, J. Rutkowska, and C. to it and so are not a test of our model of the origin of Wilson for valuable comments that greatly improved an GSD from ESD (Weibel et al. 1999; Ota et al. 2000; Devlin earlier version of the manuscript. E.A.-R. was supported and Nagahama 2002). An interesting exception is found by the National Science Foundation (IBN-0130986 and in the groupers (epinepheline serranids), where a recent IOS-1146891). phylogeny suggests that GSD of an unknown type has evolved at least three times from protogynous (ESD) an- cestry (Erisman et al. 2009). 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Karyotypic relationships among the tribes of Hypostominae diction in advance of what they might be, as in the grouper (Siluriformes: Loricariidae) with description of XO sex chromo- example above, where the prediction is ZW if females are some system in a Neotropical fish species. Genetica 128:1–9. larger in the GSD than in the protogynous species. As AmphibiaWeb. 2013. AmphibiaWeb: information on amphibian bi- modern molecular genetic approaches are extended to a ology and conservation, Berkeley, CA. Accessed February 2013. greater diversity of vertebrates, allowing discovery of sex- http://amphibiaweb.org/. Angus, R. A. 1989. A genetic overview of poeciliid fishes. Pages 51– determining systems in the absence of heteromorphic sex 68 in G. K. Meffe and F. F. Snelson, eds. Ecology and evolution chromosomes, there should be increasing opportunities of livebearing fishes (Poeciliidae). Prentice-Hall, Englewood Cliffs, for testing such predictions. 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A tokay gecko (Gekko gecko) clinging to a wall in the Calgary Zoo. This species is XX/XY, but it has close relatives that are ESD and ZZ/ ZW. Photo ᭧ 2005 Jeff Whitlock, The Online Zoo, used with permission.