The Dy Amics of a Spadefoot T Ad (Spea Multiplicata and S. Bombifrons) Hy Ridization System
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167 The Dy amics of a Spadefoot T ad (Spea multiplicata and S. bombifrons) Hy ridization System Marie A. Simovich University of San Diego and The San Diego Natural History Museum INTRODUCTION of normally efficient pre-mating isolating mecha nisms (Forester, 1969,1973; Frostand Platz, 1983; The phenomenon of hybridization has long Gartside, 1980 ; Martof, 1961). These studies have fascinated evolutionary biologists. Over the years examined how variation in factors such as habitat numerous questions concerning the geographical disturbance or breeding site condition can result in location, structure, and longevity of hybrid zones variation in the proportion of mixed-species matings. (D. Woodruff, 1973) as well as the causes and Extensive literature also addresses the role of post consequences of hybridization have been addressed mating selection, through differences in fertility, (ex. Endler, 1977, 1982; Barton, 1979; Barton and fecundity, and development on the survival of hy Hewitt, 1981, 1985; Hewitt, 1988; Moore, 1977). brid offspring (e.g. Brown, 1967; Forester, 1969, This work has revealed considerable variation in 1975; Frost, 1982 ; Sattler, 1978; Thornton, 1955). hybrid systems. Not only do systems differ from The interplay of pre- and post-mating selection, one another, but the interactions of a given species however, has seldom been evaluated directly in pair can vary spatially and/or temporally nature. In most cases, the dynamics of hybrid sys (Templeton, 1981), seemingly as a result of differ tems have been inferred from frequencies of geno ences in the responses of pure and mixed genotypes typic clas ses sampled at a single stage (usually the to the variable selectivity of spatially or temporally adult) or from breedings in the laboratory. Such patchy environments. The result is a complex or inferences may give an incomplete or even mis long-lived hybrid zone (e.g. Frost, 1982; Frost and leading picture, for, while revealing something Bagnera, 1977; Gartside, 1980; Gerhardt et al. about the result of the hybridization, single-stage 1980;Gollmann, 1991; Harrison and Arnold, 1983; samples tell us little or nothing about its cause. For Hillis, 1981; McDonnell et al. 1978; Mecham, this reason, information on the contribution of a 1960; Patton et al. 1979; Platz, 1981; Rand and number of aspects of selection operating through Harrison, 1989). These complex systems are par out the life cycle is important to the evaluation of ticularly informative because the genetic make-up hybridization systems. This paper is one part of a of each component species remains comparatively study of a complex hybrid zone between two spe uniform. This consistency makes it easier to evalu cies of spadefoot toads in Arizona. In it, pre- and ate the role of external forces (e.g., crowding, post-mating aspects of selection, including assorta habitat variation) acting both before and after mat tive mating, differences in fertility and fecundity, ing, and their effect on the outcome of hybridiza and differences in survival and developmental rate, tion. are investigated. Among anurans, numerous studies have investigated factors responsible for the breakdown la. C1 Y Herpetology of the Norl:h America~ Deserts~p p. 167-1 82 i n P. R. Brow n & S.W . Wr ig ht (eds.), Southwestern Herpetologl sts Socl et y . S 'peci al publ i cat i on #5. 168 MARIE A. SIMOVICH The System: tor/scavengers with enlarged beaks and hypertro The ranges of the spadefoot toads Spea phied jaw muscles. multiplicata and S. bombifrons overlap widely In the San Simon Valley, the ponds may h.~. (Brown, 1976; Stebbins, 1985). Although consid from three days to over two months, depending on ered to be the most distantly related species within their size and the amount of rainfall. Inyears of low the genus (see for discussion Wiens and Titus, or patchy rainfall, however, ponds frequently dry 199 1), the species are known to hybridize in a before all or sometimes any tadpoles metamorphose num ber of areas to varying extents (Brown, 1976; (Pomeroy, 1981, personal observation). Also, the Forester, 1973; Hughes, 1965; Sattler, 1978, 1985), tadpoles are exposed to a number of predators, resulting in a complex hybrid system. One OJ these another source of high mortality, and there is pre areas, the San Simon Valley of southeastern Ari sumably significant selection pressure for rapid de zona, is part of a suture zone (sensu Remmington, velopment (Caldwell et al., 1980; Creuser and 1968), an area where biomes intergrade and conge Whitford, 1976;Crump, 1989; Licht, 1974; Mayhew, ners meet and frequently hybridize. The valley itself 1965; Newman, 1988a, 1988b ;Sarnlitsch and Wilbur, has a large number of ponds and cattle tanks where 1988 ;Travis, 1980, 1983; Wilbur, 1977; Wilbur and the toads breed. Collins, 1973; Woodward, 1987). Any differences Breeding in ephemeral desert ponds con in development between pure or mixed genotypes strains the spadefoot's life cycle into precise should be exposed to immediate selection. synchrony with a very temporary aquatic environ Several aspects of the hybridization of these ment. The toads breed "explosively" (Wells, 1977), species facilitate the study of this system. First, the emerging from their burrows and going to tempo pure species, hybrids, and backcrossed individuals rary ponds and playas that fill on the first night of are easily and accurately identifiableelectrophoreti heavy summer rains (Bragg, 1965; Dimmitt and cally (Simovich, 1985). Second, the toads breed Ruibal, 1980; Forester, 1969; Ruibal et al. 1969). essentially on one night, allowing adults to be id The breeding congresses that form are often dense tified. Third, cohorts of tadpoles can be sampled and contain both species (some contain other genera repeatedly to metamorphosis, and comparisons be oftoads as well) (Bragg, 1965; Brown, 1976; Creuser tween stages can be made to assess the success of the and Whitford, 1976), taking part in what has been various pure and mixed types with respect to several termed "scramble competition" for mates (Wells, factors of selection. 1977). The females respond positivel y to the calls of conspecific males, and the males of the two species Background: call from different positions in the pond (Forester, Other investigations of this system (see 1969, 1975). Males are quite indiscriminate and will Simovich, 1985; Simovich and Sassaman, 1986; mate with either species or hybrids (Blair, 1958; Simovich, et al., 1991) provided the background Bragg, 1965; and personal observation). Under data for the present study. First, protocols were theseconditions, the effectiveness ofcall and calling established to identify genetic classes (pure species, position as mechanisms of assortative mating may hybrids, etc.) by means ofallozymes (Simovich and be much reduced (Wasserman, 1957; Wells, 1977), Sassaman, 1986). The distribution of geneticclasses and females may be grabbed by an incorrect male en in populations of tadpoles in 27 ponds in the valley route to a conspecific. was then determined over a three-year period. The The eggs are laid during the breeding con frequency of genetic classes was found to vary both gress and hatch the next day. The tadpoles develop from pond to pond and within a pond from cohort to and metamorphose in just three to four weeks. The cohort. While pure S. multiplicata was generally the tadpoles of these two species are dimorphic, occur most common class, in some ponds the two pure ring in an omnivore or a carnivore morph (see species were equally abundant. The frequenc Pomeroy, 1981). Omnivores are scavenger/grazers the hybrid classes varied from 0 to 40% (Simovicn, of normal morphology, while carnivores are preda 1985). Southwestern Herpetologists Society SPADEFOOT TOAD HYBRIDIZAnON 169 The role of pre-mating isolation was also typic class at numerous points in the cycle. addressed. Breeding adults were sampled in several breeding congresses. Assortative mating was effi METHODS cient in large or uncrowded ponds; there were few mismatches, and few hybrid tadpoles resulted. Over three years, toads in three ponds were Crowded breeding conditions (due to low rainfall or sampled periodically to metamorphosis. Six more the use of small ponds) decreased the efficiency of cohorts at two other ponds were sampled for at least assortative mating, increased mismatching, and in some consecutive post-breeding stages. Ponds are creased the generation of hybrids and backcrossed coded and locations are given in Simovich (1985). offspring. Most of the backcrosses resulted from a Figure 1, a schematic outline ofthe anuran life cycle, maleS. multiplicata (themorecommon ofthe paren indicates the stages sampled and used in predicting tal species) mating with a female hybrid. Although values, as well as the relevant stage comparisons the frequency of the mixed-genotype classes in made to determine differential performance of ge tadpoles was correlated with the frequency of mis notypic classes for the several points in the life matches by breeding adults, the proportion ofhybrid cycle. tadpole types could not be predicted precisely solely These classes are defined and abbreviated as from the degree of adult mispairing. The discrep pure S. multiplicata (M), pure S. bombifrons (B), ancy suggested that there was selection after as well hybrid (H referring to F! hybrids only) backcross to as before mating (Simovich, 1985). S. multiplicatus (BKM), backcross to S. bombifrons Analysis of intraspecific and interspecific (BKB), and double backcrosses (DBK), the off crosses from this area (Sirnovich et al., 1991) showed spring of two or more backcrosses. "Mixed" denotes that hybrid males are sterile and that hybrid females, hybrids plus all backcross classes. All animals were although fertile in backcrosses, produce only 45% as identified to genotype by electrophoresis of tissue many eggs as the pure species produce. This differ samples, which were scored for four allozyme sys ence in reproductive potential could affect the fre tems representing four unlinked diagnostic gene loci quency of tadpole classes by limiting the production (Simovich and Sassaman, 1986).