VRIJENHOEKcause alterati<strong>on</strong> of meiosis often leads to infertility or completesterility (see Templet<strong>on</strong>, 1982).Hybrid <strong>origins</strong> of unisexual vertebrates.- The hybrid natureof most unisexual vertebrates is well documented by morphological,cyto<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>, <str<strong>on</strong>g>and</str<strong>on</strong>g> electrophoretic studies (Vrijenhoek etal., this volume, <str<strong>on</strong>g>and</str<strong>on</strong>g> references <strong>the</strong>rein). The coupling betweenhybridity <str<strong>on</strong>g>and</str<strong>on</strong>g> unisexuality probably occurs because interspecifichybridizati<strong>on</strong> often disrupts normal meiosis (Schultz,1969; White, 1978; We<strong>the</strong>ringt<strong>on</strong> et al., 1987; Dawley, 1987;Moritz et al., this volume; but see Cuellar, 1974). Cytologicalmechanisms that circumvent or preclude synapsis between heterospecificchromosomes might rescue egg producti<strong>on</strong> in hybrids<str<strong>on</strong>g>and</str<strong>on</strong>g> <strong>the</strong>reby lead to n<strong>on</strong>recombinant reproducti<strong>on</strong> (Mac-Gregor <str<strong>on</strong>g>and</str<strong>on</strong>g> Uzzell, 1964; Cuellar, 1971; Cimino, 1972a, 1972b;M<strong>on</strong>aco et al., 1984).In many cases, <strong>the</strong> sexual ancestors of unisexual hybrids aremorphologically or cyto<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>ally identifiable. Never<strong>the</strong>less,allozyme studies indicate that <strong>the</strong>re is no c<strong>on</strong>sistent degree of<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> differentiati<strong>on</strong> between <strong>the</strong> sexual progenitors of unisexuallineages. For example, <strong>the</strong> sexual ancestors of Menidiaclarkhubsii exhibit a Nei's <str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> distance (D) of <strong>on</strong>ly 0.14,whereas for <strong>the</strong> sexual ancestors of unisexual Cnemidophorus,D averages 0.73 (Echelle et al., 1983; see also Moritz et al., thisvolume). This range of D values is not surprising, because noc<strong>on</strong>sistent level of <str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> differentiati<strong>on</strong> is associated withspeciati<strong>on</strong> in vertebrates (Nei, 1987). Nei's D values rangefrom 0.01 for some species pairs of birds to 3.00 for some salam<str<strong>on</strong>g>and</str<strong>on</strong>g>erpairs (Avise et al., 1980; Hight<strong>on</strong> <str<strong>on</strong>g>and</str<strong>on</strong>g> Lars<strong>on</strong>, 1979).Never<strong>the</strong>less, allopatric populati<strong>on</strong>s are likely to accumulate<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> differences that may lead to sterility in some hybrids,to various degrees of fertility in o<strong>the</strong>r hybrids, <str<strong>on</strong>g>and</str<strong>on</strong>g> to unisexualityin yet o<strong>the</strong>rs (Schultz, 1973; Berger, 1971; Vrijenhoek<str<strong>on</strong>g>and</str<strong>on</strong>g> Schultz, 1974; Turner et al., 1980; Echelle et al., 1983;Hotz et al., 1985; We<strong>the</strong>ringt<strong>on</strong> et al., 1987). Hybrid inducti<strong>on</strong>of unisexuality is ultimately a <str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> ra<strong>the</strong>r than a tax<strong>on</strong>omicproblem. Cytological <str<strong>on</strong>g>and</str<strong>on</strong>g> molecular <str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> studies of<strong>the</strong> factors involved in <strong>the</strong> inducti<strong>on</strong> of unisexuality shouldprovide a rich source of new informati<strong>on</strong> <strong>on</strong> chromosomal dynamicsduring gametogenesis.Hybridizati<strong>on</strong> is clearly <strong>the</strong> most comm<strong>on</strong> vehicle for <strong>the</strong> originof unisexual vertebrates, but it might not be <strong>the</strong> <strong>on</strong>ly <strong>on</strong>e.Electrophoretic studies suggest that par<strong>the</strong>no<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> forms of<strong>the</strong> xantusid lizard Lepidophyma flavimauclatum might havearisen sp<strong>on</strong>taneously within sexual lineages (R. Bezy, pers.comm.; see also Peccinini-Seale, this volume). Hybridizati<strong>on</strong>clearly is not necessary for <strong>the</strong> origin of many par<strong>the</strong>no<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>insects (Suomalainen et al., 1987). Underst<str<strong>on</strong>g>and</str<strong>on</strong>g>ing <strong>the</strong> <str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>factors that induce sp<strong>on</strong>taneous par<strong>the</strong>nogenesis may prove tobe an even more difficult but never<strong>the</strong>less rewarding task (seeTemplet<strong>on</strong>, 1982).Syn<strong>the</strong>tic unisexuals.- Schultz (1973) accomplished <strong>the</strong> firstsuccessful syn<strong>the</strong>sis of a unisexual vertebrate in <strong>the</strong> laboratory.He reproduced <strong>the</strong> origin of <strong>the</strong> hybrido<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> fish Poeciliopsism<strong>on</strong>acha-lucida through crosses of P. m<strong>on</strong>acha femaleswith P. lucida males. We<strong>the</strong>ringt<strong>on</strong> et al., (1987) found thatcrosses of P. m<strong>on</strong>acha females with P. occidentalis males havea higher success rate for producing new hybrido<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>strains. Regardless of <strong>the</strong> geographical origin of <strong>the</strong> parents,all <strong>the</strong> m<strong>on</strong>acha x occidentalis hybrids were females, <str<strong>on</strong>g>and</str<strong>on</strong>g> all<strong>the</strong> fertile hybrids were also sp<strong>on</strong>taneously hybrido<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>.Hybridogenesis in Poeciliopsis appears to be induced by genomicinteracti<strong>on</strong>s, not specific factors restricted to a few geographicallocati<strong>on</strong>s. Attempts to reproduce <strong>the</strong> origin of <strong>the</strong>gyno<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> fish Roecilia formosa through crosses of P. mexicana<str<strong>on</strong>g>and</str<strong>on</strong>g> P. latipinna have been unsuccessful, producing <strong>on</strong>lysterile hybrids or hybrids with normal meiosis. Turner et al.(1980) suggested that <strong>the</strong> specific genomes or individual genesthat induced gynogenesis in Poecilia formosa might be restrictedto a few populati<strong>on</strong>s that have not yet been tested orwhich, perhaps, may no l<strong>on</strong>ger exist. Rec<strong>on</strong>structi<strong>on</strong> of <strong>the</strong> <strong>origins</strong>of <strong>the</strong> hybrido<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> frog Rana esculenta through crossesof Rana ridibunda x R. less<strong>on</strong>ae also had a str<strong>on</strong>g geographicalbasis. Some of <strong>the</strong> ridibunda x less<strong>on</strong>ae hybrids were hybrido<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>,<str<strong>on</strong>g>and</str<strong>on</strong>g> o<strong>the</strong>rs had normal meiosis (Hotz et al., 1985).Studies of mitoch<strong>on</strong>drial DNA in unisexual lizards also suggestthat opportunities for <strong>the</strong> origin of new unisexual strainsmay be restricted to a few progenitors or perhaps a few geographicalpopulati<strong>on</strong>s (Moritz et al., this volume).Developmental <str<strong>on</strong>g>c<strong>on</strong>straints</str<strong>on</strong>g>.- A severe c<strong>on</strong>straint <strong>on</strong> hybrid <strong>origins</strong>of unisexual vertebrates results from <strong>the</strong> need for a delicatebalance between <strong>the</strong> disrupti<strong>on</strong> of normal gametogenesis<str<strong>on</strong>g>and</str<strong>on</strong>g> <strong>the</strong> coordinati<strong>on</strong> of normal development in hybrids (Vrijenhoek<str<strong>on</strong>g>and</str<strong>on</strong>g> Lerman, 1982; We<strong>the</strong>ringt<strong>on</strong> et al., 1987). Hybridizingentities must be dissimilar enough to disrupt meiosis<str<strong>on</strong>g>and</str<strong>on</strong>g> yet not so dissimilar that somatic development ofhybrids is also disrupted. Moritz et al. (this volume) call this<strong>the</strong> "balance" hypo<strong>the</strong>sis. We<strong>the</strong>ringt<strong>on</strong> et al. (1987) examineddevelopmental abnormalities in laboratory-syn<strong>the</strong>sized hybrido<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>strains of Poeciliopsis m<strong>on</strong>acha-lucida. A majority of16 viable strains exhibited some birth defects in <strong>the</strong> form ofcranial <str<strong>on</strong>g>and</str<strong>on</strong>g> spinal deformities. Although <strong>on</strong>ly a small proporti<strong>on</strong>of <strong>the</strong> individuals within each strain (maximum 7%) werevisibly deformed, <strong>the</strong>se abnormalities were probably symptomaticof a general weakening of developmental homeostasis.We saw no comparable birth defects in <strong>the</strong> sexual ancestors of<strong>the</strong>se hybrids. Most importantly, <strong>the</strong> syn<strong>the</strong>tic unisexual hybridshad, <strong>on</strong> average, significantly lower fertility <str<strong>on</strong>g>and</str<strong>on</strong>g> survivalthan <strong>the</strong> parental strains. Never<strong>the</strong>less, several of <strong>the</strong> syn<strong>the</strong>ticunisexuals exhibited no evidence of birth defects <str<strong>on</strong>g>and</str<strong>on</strong>g><strong>the</strong>ir fertility <str<strong>on</strong>g>and</str<strong>on</strong>g> survival was not different from that of <strong>the</strong>sexual ancestors. These 16 strains represent <strong>the</strong> survivorsfrom 33 syn<strong>the</strong>tic strains. The o<strong>the</strong>r strains could not be sustainedbey<strong>on</strong>d <strong>the</strong> sec<strong>on</strong>d or third laboratory generati<strong>on</strong> becauseof low viability <str<strong>on</strong>g>and</str<strong>on</strong>g> fertility. Intense fertility <str<strong>on</strong>g>and</str<strong>on</strong>g> viability"bottlenecks" also occurred during <strong>the</strong> formati<strong>on</strong> of newpar<strong>the</strong>no<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> lineages of Drosophila mercatorum (Templet<strong>on</strong>,1982). Only a few lucky genotypes strike <strong>the</strong> proper balancebetween meiotic disrupti<strong>on</strong> <str<strong>on</strong>g>and</str<strong>on</strong>g> developmental coordinati<strong>on</strong>.Sperm-dependence.- Pseudogamy (false fertilizati<strong>on</strong>) imposessevere reproductive <str<strong>on</strong>g>and</str<strong>on</strong>g> <str<strong>on</strong>g>ecological</str<strong>on</strong>g> <str<strong>on</strong>g>c<strong>on</strong>straints</str<strong>on</strong>g> <strong>on</strong> <strong>the</strong> establishmentof gyno<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> fishes <str<strong>on</strong>g>and</str<strong>on</strong>g> amphibians, because itforces unisexuals into parasitic relati<strong>on</strong>ship with a closely relatedbisexual species. The <strong>on</strong>ly truly par<strong>the</strong>no<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> vertebratesare reptiles. Why unisexual fishes <str<strong>on</strong>g>and</str<strong>on</strong>g> amphibianshave been unable to shed <strong>the</strong> burden of sperm-dependence is25
CONSTRAINTS ON UNISEXUAL VERTEBRATESunclear (Uzzell, 1970). We do not know what happens to <strong>the</strong>sperm pr<strong>on</strong>ucleus after activati<strong>on</strong> of gyno<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> eggs, or hownuclear fusi<strong>on</strong> is blocked. Fur<strong>the</strong>rmore, we do not know howcleavage is activated in par<strong>the</strong>no<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> reptiles. The origin ofnew par<strong>the</strong>no<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> reptiles might be severely c<strong>on</strong>strainedbecause an endogenous mechanism to activate embryogenesismust arise simultaneously with a mechanism that circumventsnormal meiosis. Unless both mechanisms are byproductsof <strong>the</strong> same dysgenic event (e.g., hybridizati<strong>on</strong>), <strong>the</strong>origin of new par<strong>the</strong>nogens seems very unlikely. Despite <strong>the</strong>c<strong>on</strong>siderable effort over <strong>the</strong> past 50 years, fundamental cyto<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g><str<strong>on</strong>g>and</str<strong>on</strong>g> <strong>on</strong>to<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> processes are still unknown to us. Studiesof <strong>the</strong>se aberrant processes in unisexual organisms shouldserve as excellent tools for elucidating critical aspects of normalfertilizati<strong>on</strong> <str<strong>on</strong>g>and</str<strong>on</strong>g> early development.Hybrido<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> unisexuals also require sperm from males ofa related sexual species, but <strong>the</strong>y are not truly pseudogamous,because <strong>the</strong> egg <str<strong>on</strong>g>and</str<strong>on</strong>g> sperm pr<strong>on</strong>ucleii fuse <str<strong>on</strong>g>and</str<strong>on</strong>g> a true hybrid isformed. During hybrido<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> reproducti<strong>on</strong>, <strong>on</strong>ly <strong>the</strong> haploidmaternal genome is transmitted to <strong>the</strong> eggs without recombinati<strong>on</strong>(Schultz, 1969; Uzzell <str<strong>on</strong>g>and</str<strong>on</strong>g> Berger, 1975; Graf <str<strong>on</strong>g>and</str<strong>on</strong>g> Polls,this volume). This form of reproducti<strong>on</strong> has been called "hemicl<strong>on</strong>al"(Kailman, cit. in Vrijenhoek et al., 1977). Because hybridogensare also sperm-dependent, <strong>the</strong>y also suffer <strong>the</strong>pseudogamy c<strong>on</strong>straint.'lb appreciate <strong>the</strong> severity of this c<strong>on</strong>straint, we must imaginea pair of bisexual species with c<strong>on</strong>specific mating preferences.If, for example, interspecific matings occur <strong>on</strong>ce in every100 courtships, <str<strong>on</strong>g>and</str<strong>on</strong>g> if <strong>the</strong> resulting unisexual hybrids are exactlyintermediate in <strong>the</strong>ir attractiveness to males, <strong>the</strong> hybridswould be mated <strong>on</strong>ce in every 50 courtships. It is difficultto imagine a pseudogamous form successfully invading a bisexualpopulati<strong>on</strong> under such c<strong>on</strong>diti<strong>on</strong>s. Special behavioralc<strong>on</strong>diti<strong>on</strong>s must exist in <strong>the</strong> sexual host before pseudogamousunisexuals can become established. For example, traits involvedin mate selecti<strong>on</strong> might not be additive in some hybrids,placing <strong>the</strong> hybrids bey<strong>on</strong>d a critical mate-selecti<strong>on</strong>threshold. However, behavioral studies with Poeciliopsis revealedthat <strong>the</strong> situati<strong>on</strong> is more complex. The unisexuals exploit<strong>the</strong> dominance hierarchies formed by sexual males(McKay, 1971). Dominant males prevent subordinate malesfrom mating with <strong>the</strong> preferred bisexual females, <str<strong>on</strong>g>and</str<strong>on</strong>g> thus <strong>the</strong>subordinate males defer <strong>the</strong>ir mating attempts to unisexualfemales.Having invaded a bisexual populati<strong>on</strong>, pseudogamous unisexualsface a sec<strong>on</strong>d peril — <strong>the</strong> twofold advantage of allfemalereproducti<strong>on</strong> should lead to <strong>the</strong>ir own demise (Clant<strong>on</strong>,1934). Assuming unisexual <str<strong>on</strong>g>and</str<strong>on</strong>g> bisexual forms occupy equivalentniches, <strong>the</strong> unisexuals should rapidly replace <strong>the</strong> bisexuals,<strong>the</strong>reby eliminating <strong>the</strong>ir source of sperm. The persistenceof stable unisexual/bisexual complexes has beenexplored by several investigators (Uzzell, 1964, 1969; Moore<str<strong>on</strong>g>and</str<strong>on</strong>g> McKay, 1971; Moore, 1976, 1984; Kiester et al., 1981;Keegan-Rogers, 1984; Stenseth et al., 1985). Based <strong>on</strong> studiesof gyno<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> Poeciliopsis, Moore (1976) identified three factorsaffecting <strong>the</strong> dynamics of this simple host-parasite system:(1) primary fitness (i.e., fertility <str<strong>on</strong>g>and</str<strong>on</strong>g> survival), (2) <strong>the</strong> twofoldadvantage of all-female reproducti<strong>on</strong>, <str<strong>on</strong>g>and</str<strong>on</strong>g> (3) afrequency-dependent mating preference <strong>on</strong> <strong>the</strong> part of sexualmales. Assuming equal primary fitnesses <str<strong>on</strong>g>and</str<strong>on</strong>g> equal niches,Moore showed how factors 2 <str<strong>on</strong>g>and</str<strong>on</strong>g> 3 could lead to a stable equilibriumbetween unisexual <str<strong>on</strong>g>and</str<strong>on</strong>g> bisexual forms. When bisexualindividuals predominate, <strong>the</strong> males establish dominancehierarchies, <str<strong>on</strong>g>and</str<strong>on</strong>g> <strong>the</strong> subordinate males mate with <strong>the</strong> unisexuals.As <strong>the</strong> unisexual females increase in frequency becauseof <strong>the</strong>ir twofold advantage, males become scarce. Solitarymales prefer <strong>the</strong>ir c<strong>on</strong>specific bisexual females, <str<strong>on</strong>g>and</str<strong>on</strong>g> thus unisexualfemales have a low probability of inseminati<strong>on</strong>. At equilibrium<strong>the</strong> two-fold advantage of unisexuals is balanced by<strong>the</strong>ir lowered mating success. The c<strong>on</strong>diti<strong>on</strong>s necessary forstable coexistence between a sperm parasite <str<strong>on</strong>g>and</str<strong>on</strong>g> its sexualhost are restrictive (Stenseth et al., 1985; Kirkendall <str<strong>on</strong>g>and</str<strong>on</strong>g>Stenseth, 1988). Some form of density- or frequencydependent,unisexual mating success appears to be a generalrequirement. Also, <strong>the</strong> assumpti<strong>on</strong>s of equal primary fitnesses<str<strong>on</strong>g>and</str<strong>on</strong>g> completely overlapping <str<strong>on</strong>g>ecological</str<strong>on</strong>g> niches are probably unrealistic(Vrijenhoek, 1978; Moore, 1984; Schenck <str<strong>on</strong>g>and</str<strong>on</strong>g> Vrijenhoek,1986).IT'S HARD TO FIND A JOB ASA UNISEXUAL VERTEBRATEEcological weeds.- The <str<strong>on</strong>g>ecological</str<strong>on</strong>g> problems faced by unisexualvertebrates have received c<strong>on</strong>siderable attenti<strong>on</strong>. Pseudogamousunisexuals suffer <strong>the</strong> most severe c<strong>on</strong>straint, because<strong>the</strong>se sperm parasites cannot escape from, or outcompete,<strong>the</strong>ir sexual hosts. True par<strong>the</strong>nogens, however, are free toplay <strong>the</strong> role of fugitive species, relying <strong>on</strong> superior col<strong>on</strong>izati<strong>on</strong>ability <str<strong>on</strong>g>and</str<strong>on</strong>g> a potential for rapid increase attributable toall-female reproducti<strong>on</strong>. Par<strong>the</strong>no<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g> forms of Cnemidophorusmay be <strong>the</strong> zoological equivalents of "weedy species"(Wright <str<strong>on</strong>g>and</str<strong>on</strong>g> Lowe, 1968), having a high intrinsic rate of increase<str<strong>on</strong>g>and</str<strong>on</strong>g> excepti<strong>on</strong>al col<strong>on</strong>izing abilities (Maslin, 1971). Theweeds hypo<strong>the</strong>sis assumes par<strong>the</strong>nogens are inferior competitorswithin <strong>the</strong> natural habitats of <strong>the</strong> parental species (Moore,1984). The successful establishment of weedy par<strong>the</strong>no<str<strong>on</strong>g>ge<strong>net</strong>ic</str<strong>on</strong>g>forms depends up<strong>on</strong> <strong>the</strong> availability of disturbed (disclimax) ormarginal habitats in which <strong>the</strong> parental forms are inferiorcompetitors (Cuellar, 1977a). Because of worldwide habitat destructi<strong>on</strong>due to human activities, Suomalainen et al. (1987, p.199) jestingly suggested <strong>the</strong> future may not be so hopeless forpar<strong>the</strong>nogens that "thrive in disturbed habitats <str<strong>on</strong>g>and</str<strong>on</strong>g>. . . toleratepolluti<strong>on</strong> better than bisexuals?'Hybridizati<strong>on</strong> <str<strong>on</strong>g>and</str<strong>on</strong>g> an intermediate niche.- A variant of <strong>the</strong>weeds hypo<strong>the</strong>sis is <strong>the</strong> intermediate niche hypo<strong>the</strong>sis (Moore,1984). Because hybrids tend to be intermediate in morphology<str<strong>on</strong>g>and</str<strong>on</strong>g> presumably o<strong>the</strong>r characteristics that would c<strong>on</strong>strain<strong>the</strong>ir ability to use food <str<strong>on</strong>g>and</str<strong>on</strong>g> spatial resources, unisexual hybridsmight be best suited for ecot<strong>on</strong>al regi<strong>on</strong>s or intermediateniches in which <strong>the</strong> parental species are inferior competitors.This hypo<strong>the</strong>sis assumes <strong>the</strong> parental species are eachadapted to different regi<strong>on</strong>s al<strong>on</strong>g an <str<strong>on</strong>g>ecological</str<strong>on</strong>g> gradient. Althoughhybrid intermediacy may play a role in c<strong>on</strong>straining<strong>the</strong> broad-scale geographical distributi<strong>on</strong> of some unisexualhybrids (Moore, 1984), factors affecting <strong>the</strong> local distributi<strong>on</strong>26