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REPRODUCTIVE MECHANISM of UNISEXUAL and BISEXUAL STRAINS of the VIVIPAROUS FISH Poeciliopsisl

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REPRODUCTIVE MECHANISM of UNISEXUAL and BISEXUAL STRAINS of the VIVIPAROUS FISH Poeciliopsisl REPRODUCTIVE MECHANISM OF UNISEXUAL AND BISEXUAL STRAINS OF THE VIVIPAROUS FISH POECILIOPSISl R. JACK SCHULTZ Museum of Zoology, The University of Michigan Received September 12, 1960 The fishes of the order Cyprinodonti­ one or two uneven rows that follow the formes have evolved a variety of systems heart-shaped curvature of the lips and the of sex-determination, some of which are outer row of teeth. The second type of unique among vertebrate animals. One dentition is characteristic of an aberrant such anomalous condition was recently re­ strain of "F" females which are designated ported by Miller and Schultz (1959) in the as "Fx." The inner teeth of this strain viviparous genus Poeciliopsis Regan, where­ consist of a fine sandpaper-like patch on in certain strains gave birth to only female either side of the midline. No other con­ offspring. Poeciliopsis comprises approxi­ sistent morphological differences have been mately 16 species that range from southern found between the two strains, yet repro­ Arizona to Colombia, with at least two ductively they are radically different. Mat­ endemics in the Atlantic drainage of the ings of "F" females having normal denti­ Isthmus of Tehuantepec (fig. 1). Western tion to "F" males result in young of both Mexico harbors the largest number of sexes, but the "Fx " females with aberrant species. dentition mated to the same male produce This study deals principally with two only female progeny. species of Poecdiopsis tentatively assigned The same aberrant dental character was to the species group Leptorhaphis Regan later found in samples of strain "c." In (Miller, 1960). Since neither species has these, however, dentition proved to be less been described.f they are here assigned the reliable for distinguishing the unisexual symbolic designations "C" and "F." Poe­ strain, designated "C x ," from the normal ciliopsis "C" is found in southern Sonora females. Offspring from "C x " individuals and northern Sinaloa, where it is confined showed a spectrum of variation from the to the Mocorito, Sinaloa, and Fuerte river nearly normal to the aberrant types of drainages. The southern limit of "F" is dentition. These progeny were nevertheless less than 50 miles to the north; it extends all females, as were the succeeding genera­ from the Rio Mayo northward to the tions. Yaqui, Matape, Sonora, and Concepcion This "all-female" phenomenon appears rivers in Sonora. to be similar to that discovered by Hubbs From preserved material collected within and Hubbs (1932) in Mollienesia formosa, the range of strain "F," Miller was able a member of the same family as Poe­ to identify females with two types of denti­ ciliopsis. tion. One of these is considered to be the It is the purpose of this study to find normal type in that the minute inner teeth the sex-determining mechanism responsible are like those of the male. They consist of for unisexuality in Poeciliopsis. Aspects of 1 Part of a thesis submitted to The University the reproductive biology and genetics of of Michigan in partial fulfillment of the require­ both the bisexual and the unisexual types, ments for the degree of Doctor of Philosophy, therefore, have been studied and compari­ June, 1960. Cost of extra pages paid for by the author. sons have been made with other animals 2 Since this was written, the species here re­ known to have unusual sex-ratios. The fol­ ferred to "C" and "Cx" has been described as lowing mechanisms have been considered: Poeciliopsis lucida; the one designated "F" and lethal systems, polyploidy, parthenogenesis, "Fx" may be identical with P. occidentalis (Miller, 1960) . gynogenesis, sex-inversion, cytoplasmic in- EVOLUTION 15: 302-325. September, 1961 302 REPRODUCTIVE MECHANISM OF POECILIOPSIS 303 20' / II POEClLlOPS1S ·c-cx Ea POECILIOPSIS 'f- f~ [J ALL OTHERS ..' FIG. 1. Distribution of Poeciliopsis in part of North America, showing localities from which live stocks were obtained. heritance, unbalanced autosomal system, cated in fig. 1 by collecting station num­ and selective maturation. bers. Specimens to be used for genetic analysis MATERIALS AND METHODS or to be dissected for gonadal studies were Live stocks used in this investigation fixed in 10% formalin and preserved in were collected in northwestern Mexico dur­ 70% ethyl alcohol. Examination of live ing expeditions by Miller and Greenbank material was facilitated by the use of an in 1955, Miller and Miller in 1957, and anesthetic, MS-222 (Tricaine methane­ Miller and Schultz in 1959. The localities sulfonate). Immature fish used in histo­ from which they were obtained are indi- logical studies were killed and fixed in 304 R. JACK SCHULTZ Bouin's solution and preserved in 70% completion of yolk deposition, it migrates alcohol. The entire fish was embedded in to the periphery, where maturation division paraffin and sections were cut at 10 mi­ occurs. crons. These were stained in Ehrlich's After this series of eggs is fertilized, haematoxylin and counterstained with eosin, yolk accumulates in a second series. By and were examined at magnifications of the time the first embryos are 7 to 10 days 430x and 980x. Cytological preparations old and have reached the halfway point in were made from embryos one or two days their development, the second series of ova old and from testes of adult males. The is fertilized. In strains "C" and "Cx" the tissue was killed and fixed in Newcomer's blastula or streak stage of a third brood of solution, stained in aceto-carmine and embryos is sometimes found before the squashed between cover slip and slide. All birth of the first or oldest stage of embryos, fish measurements are the total length in but in "F" and "Fx" no more than two mm estimated to the nearest tenth. stages of embryos occur at one time. If sperm are not available to fertilize the REPRODUCTIVE BIOLOGY newly matured ova the condition does not Insemination.-Poeciliopsis, being a vi­ remain static but degeneration of the ova viparous fish, has internal fertilization. ensues. Degenerating ova and embryos are Spermatophores or sperm packets are common in females living under subopti­ placed in the genital pore of the female mum conditions or in those used in certain by means of the male's modified anal fin, hybrid crosses. Frequently one to several the gonopodium. Here, the packets break ova of a clutch fail to become fertilized or up, releasing the spermatozoa. These mi­ an embryo dies in the course of its develop­ grate up the gonaduct to the ovary where ment. The age of these can be correlated they remain viable for months. As a re­ with the brood of embryos of which they sult of sperm storage, Poeciliopsis females normally would have been a part. Degen­ may produce as many as ten broods of erating elements in the ovary can be recog­ young after they have been isolated from nized for more than two weeks after their their mates. death. Ovarian Cycle.-Most viviparous fishes In dealing with unisexual animals, one have only one stage of embryos in the of the concerns is whether or not the one ovary at a time: the birth of these must sex dies before maturity. A more complete take place before the next series of ova is evaluation of lethals as they relate to the fertilized. Poeciliopsis, however, has super­ unisexual strains of Poeciliopsis will be fetation, wherein two or more stages of considered later, but certain aspects that embryos develop simultaneously (Turner, involve the ovary are treated appropriately 1937) . here. From the brood records and from the In a reproductive system such as that of examination of more than 400 females, a viviparous fishes, a lethal mechanism acting generalized sequence of events occurring during the intraovarian cycle would reveal within the ovary has been reconstructed. itself by the presence of dead embryos, Except for minor deviations it seems ap­ eggs, or oocytes. In "Cx" and "Fx," a suf­ plicable to all species of Poeciliopsis. ficient number of failures to account for Ovaries of submature females contain unisexuality might be expected at any of several strings of tiny, white oocytes, .25 the following stages of the ovarian cycle: to .30 mm in diameter. As the female ( 1) maturation division; (2) fertilization; matures, one or two of these oocytes begin (3) early cleavage; and (4) advanced em­ to accumulate yolk, which gives them an bryos. In "C" and "F" no more than a few amber color. The nucleus is centrally lo­ prenatal deaths theoretically should occur. cated in these submature eggs; but upon From the 38 "C" and "Cx" females dis- REPRODUCTIVE MECHANISM OF POECILIOPSIS 305 TABLE 1. Comparison of intraovarian mortality TABLE 2. Minimum and average brood interval between strains "C" and "Cs" in days of strains "C;" "Cs" "F," and "E," Ova and Per cent Minimum Average Strain of Number embryos of Strain of Sample brood brood female dissected observed mortality female size interval interval C 11 102 21.7 P.C 182 4 11.5 Cx 27 319 5.6 P. c, 124 7 11.7 P.F 26 5 13.8 P.Fx 76 9 13.2 sected for this phase of the study, only a few dead embryos could be found. The is retained in the ovary and is not born degenerating elements observed were for until one or two days after the others. Fe­ the most part identified as ova. Many of males in poor condition have irregular in­ these, however, were undoubtedly e~rly em­ tervals, but even healthy individuals ex­ bryos undetected because of their small perience interruption or "rest periods" after size and degenerate condition. When the a long sequence of births. Although more total intraovarian mortality of "C" and typical of winter months, long brood inter­ "Cx" was compared (table 1), the uni­ vals also may occur during the summer.
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