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Embryonic growth in the viviparous Poeciliid, Heterandria formosa
Abstract
In Heterandria formosa the fertilized eggs are minute and the embryos secure their nourishment for development through a placental type of association with the mother. This paper presents an analysis of embryonic growth in this viviparous species and a comparison of this growth with that in oviparous fishes. In the dis cussion an attempt is made to evaluate the factors restricting growth in Heterandria. A similar study of embryonic growth in a number of ovoviviparous fishes is to follow. Bailey (1933) and Turner (1937) have directed attention to the development of embryos in poeciliid fishes in relation to the mother. Turner (1940a, b, c, d) surveyed the various types of association between mother and embryo for the four viviparous Cyprinodont families (Poeciliidae, Anablepidae, Goodeidae, and Jenynsiidae). For theoviparousfishes, thework ofGray (1926,1928)on thedevelopmentof the trout Salmo fario stands almost alone. However, Kronfeld and Scheminzki (1926) have also contributed data on the trout. This work on a fish species totally dependent upon yolk for its embryonic nourishment provides the basis for the com parison and interpretation of many of the observations described below. MATERIAL Heterandria formosa is remarkable in showing a high degree of superfetation. As many as eight broods of developing embryos occur within the ovary of a single female. Active sperm are retained in the ovary for many months following a single copulation. Thus it is impossible to determine the exact time of fertilization or the time it has taken any particular brood to reach the stage in which it is found. Its embryonic development resembles in its general aspects that of Fundulus and other Cyprinodont fishes. In Heterandria, as in all poeciliid fishes, the em bryos are retained until parturition within the follicles of the single median ovary. Following fertilization the ovum and the follicle become separated by the perivitel line space and fluid. The follicular membrane is henceforth generally referred to as the ovisac. Its diameter increases with the extension of the fluid filled spaces associated with the embryo and with the growth of the embryo itself. Sections of the immature ova show little yolk, but numerous small oil globules are already present (Fig. 1). The latter increase in volume as the eggs grow, and their number is reduced by the coalescence of the small vacuoles (Fig. 2). The large oil globules fuse at the time of fertilization to form a single large spherical oil 1 The author expresses appreciation to Dr. Leigh Hoadley for suggestions and encourage ment in this work. 37
... Ten replicates, comprised of groups of five embryos or ova each, were dry-weighed for each of three to four distinct developmental stages for the five species. Scrimshaw (1945) determined that dry weights of preserved embryos (killed and fixed in 10% formalin and preserved in 70% ethanol) closely approximate dry weights of freshly killed embryos; our work substantiated this. ...
... Most poeciliids, including the well-known genera Poecilia, Gambusia, and Xiphophorus, have mature ova about 2 mm in diameter (Scrimshaw, 1946;Tavolga, 1949). Ova of this size usually contain sufficient yolk to account for the weight of the embryos at the end of their intraovarian lives except for that quantity which is spent supplying the metabolic requirements of the developing embryo (Scrimshaw, 1944a(Scrimshaw, , 1944b(Scrimshaw, , 1945. ...
... Most poeciliids, including the well-known genera Poecilia, Gambusia, and Xiphophorus, have mature ova about 2 mm in diameter (Scrimshaw, 1946;Tavolga, 1949). Ova of this size usually contain sufficient yolk to account for the weight of the embryos at the end of their intraovarian lives except for that quantity which is spent supplying the metabolic requirements of the developing embryo (Scrimshaw, 1944a(Scrimshaw, , 1944b(Scrimshaw, , 1945. ...
... ical conditions and display a variety of life history patterns (Schultz 1977, Reznick and Endler 1982, Farr 1984). The family includes species with varying degrees of clutch overlap, and poeciliid reproductive biology has been well described (Henn 1916, Turner 1937, 1940a, b, 1947, Fraser and Renton 1940, Scrimshaw 1944a, b, 1945, 1946, Colson 1969, Monaco et al. 1978,Trexler 1985, Snelsonetal. 1986). ...
... It is a small viviparous species of the southeastern United States that occupies a variety of habitats (Swift et al. 1977). Females produce small ova, and most of the energy for embryonic development is supplied directly through vascular connections between mother and embryo (Turner 1940a, Scrimshaw 1945. Preliminary investigations (Cheong et al. 1984) suggested that the plasticity of reproductive traits with respect to food level might be a key element in the expression of superfetation in this species. ...
... The distributions of these traits are consis? tent with those found in previous work (Scrimshaw 1944/?, 1945, Cheong et al. 1984. Brood size and the average size of offspring in the brood were uncorrelated (r = ?0.04), even when partialled on female body size (r= -0.12). ...
of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. Abstract. We used laboratory and field studies of the reproductive ecology of the poeciliid fish Heterandria formosa to examine the possible mechanisms that have driven the evolution of superfetation (simultaneous provision of maternal care to sets of dependent offspring in diverse stages of development). Increased food levels in the laboratory increased the number of broods that a female produced by increasing the level of superfetation. Brood sizes were determined by female body size and were unaffected by food level. Offspring size was unaffected by food level but varied with female age. Different females had different age-specific offspring sizes. Brood size and offspring size were not correlated, even when female size was held apart. In the field the level of superfetation increased with the total number of embryos, even when female size was held apart. Larger, older females displayed higher levels of superfetation than smaller, younger females. Superfetation appeared to increase offspring production rate without compromising brood size or individual offspring size. The correlations among reproductive traits that were displayed by H. formosa were quite different from those found in poeciliid fish without superfetation. Heterandria ex-hibited a demographic regime characterized by overlapping generations but high adult mortality rates relative to juvenile mortality. We used these results to test three general hypotheses for the evolution of clutch overlap. The results support Burley's (1980) hypothesis that clutch overlap is an adaptation to maximize offspring production rates in the face of limited maternal effort. We modified this hypothesis to specify production of large offspring. In poeciliids, the critical tests of this modification will involve comparing the reproductive and demographic patterns ob? served in species such as Heterandria formosa, which occupies an extreme position with regard to clutch overlap, with species such as Gambusia affinis, which does not display clutch overlap, yet is often syntopic with Heterandria. Similar comparative studies in demography could address the question of why clutch overlap is not more common.
... Such females produce broods of young more frequently than those without superfoetation. Yet, early work by Turner (1940a) and others (Scrimshaw, 1944) lacked an evolutionary perspective on the distribution and pattern of maternal life histories in Poeciliidae. The work of these earlier scientists predates the development of †Author to whom correspondence should be addressed. ...
... The conclusion that P. fairweatheri lacks superfoetation contradicts reports by Turner (1940b) and Scrimshaw (1944). A possible explanation for the contradiction is interpopulation variation in the mode of reproduction. ...
... It is also possible that an error occurred when identifying the species. Both Turner (1940b) and Scrimshaw (1944) reported results for a species named Dextripenis evides (Turner 1940) that was reclassified by Rosen & Bailey (1963) as P. fairweatheri . Without voucher specimens from Turner's or Scrimshaw's collections it is not possible to confirm their identification. ...
This study presents a description of the life histories of all four species of the genus Phallichthys, found primarily in the Atlantic slope of Central America (ranging from northern Panama to Mexico), based on a combination of data collected from preserved and living specimens. All species produced a single litter of offspring before developing another brood (i.e. no superfoetation). In the laboratory, the mean time interval between successive litters ranged from 24 to 48 days, further suggesting that they lack superfoetation. Embryos lose from 15 to 65% of their dry mass during development, meaning all or the large majority of resources required for development are provided prior to fertilization (lecithotrophy). All mature male size distributions were platykurtotic and appeared either bimodal or multimodal. Multimodal and skewed size distributions have been associated with genetic polymorphisms for size at maturity in other species of Poeciliidae. As the sister clade to Phallichthys includes genera in which all species have superfoetation (Neoheterandria and Poeciliopsis), these results suggest that their common ancestor with Phallichthys also had superfoetation and that the trait has been lost.
... Such structures are considered the primary sites of embryo-maternal metabolic interchanges, including nutrients, mainly, through the yolk sac; and gases, mainly through the pericardial sac (Depeche, 1970;Fraser & Renton, 1940;Jollie & Jollie, 1964;Scrimshaw, 1944;Turner, 1940a). Wourms (1991) considered that in specialized forms of viviparity as occurred in matrotrophy, the embryos acquire progressively maternal dependency for their nutrition. ...
... Conversely, in the matrotrophic H. formosa, the yolk is absorbed in the early stage of development and consequently, the yolk sac is extremely reduced even early gestation and absent during the rest of gestation. However, the pericardial sac of H. formosa was observed, as (Fraser & Renton, 1940;Grove & Wourms, 1991;Scrimshaw, 1944;Tavolga, 1949;Tavolga & Rugh, 1947;Thibault & Schultz, 1978;Turner, 1940aTurner, , 1947Wourms et al., 1988) and with recent studies in other matrotrophic poeciliids (Olivera-Tlahuel et al., 2019). The differences between lecithotrophic and matrotrophic species in the contribution of the pericardial sac to the embryonic vascularized surface found in this study are consistent with those described by Wourms et al. (1988). ...
We used histological techniques to describe the morphology of the yolk and pericardial sacs in developing embryos of the lecithotrophic species Girardinus creolus, Gambusia puncticulata, Limia vittata and Quintana atrizona, in comparison with the extreme matrotrophic Heterandria formosa. In lecithotrophic species, the yolk sac was enlarged and lasted until the final stages of development, while in H. formosa it was completely absorbed soon after fertilization. Lecithotrophic poeciliids showed a pericardial sac with a single layer of blood vessels covering the dorsal surface of the cephalic region only, whilst H. formosa showed a more complex largely vascularized pericardial sac covering the entire dorsal surface, except the caudal region. In advanced gestation of G. creolus, a vascular plexus of the yolk sac reaches the pharyngeal region, behind the gills, suggesting that the pharynx may play a role in embryonic nutrition in lecithotrophic species. These morphological evidences suggest that matrotrophy derives from lecithotrophy.
... Apparently, superfetation has evolved independently several times within the Poeciliidae (Meredith, Pires, Reznick, & Springer, 2011;Pires, Banet, Pollux, & Reznick, 2011;Pollux, Pires, Banet, & Reznick, 2009). Some species have a high degree of superfetation; for example, H. formosa can carry up to eight simultaneous broods, each at a different developmental stage (Scrimshaw, 1944). Other species, such as Poeciliopsis turrubarensis, have a lower degree of superfetation, and can only carry two or three simultaneous broods (Z uñiga-Vega, Reznick, & Johnson, 2007). ...
... However, there are studies that provide information about how long spermatozoa remain viable within the ovary, which is indirect evidence of the time between the formation and disappearance of spermathecae. For example, sperm may be stored for up to nine months in H. formosa and up to 10 months in H. dactylopterus (Fraser & Renton, 1940;Hubbs, 1964Hubbs, , 1997Scrimshaw, 1944;Vila et al., 2007). Other vertebrates exhibit structures analogous to the spermathecae of poeciliid fishes (Dallai, 1975;Holt & Lloyd, 2010;Palmer, Rostal, Grumbles, & Mulvey, 1998;Suarez, 2008). ...
Sperm storage within the female reproductive tract has been reported as a reproductive strategy in several species of vertebrates and invertebrates. However, the morphological structures that allow for sperm to be stored and kept viable for long periods are relatively unknown in osteichthyes. We use histological and stereological tools to identify and quantify sperm storage structures (spermathecae) in 12 species of viviparous Poeciliidae. We found spermathecae in nine species, six of which exhibit superfetation (the ability of females to simultaneously carry within the ovary two or more broods of embryos at different stages of development). These spermathecae are folds of ovarian tissue that close around spermatozoa. We compared the number and size (volume) of spermathecae between species with and without superfetation. Species that exhibit superfetation had a significantly higher number of spermathecae than species that do not exhibit this reproductive strategy. In addition, we found that the mean volume of spermathecae and total volume of spermathecae present in the ovary are marginally higher in species with superfetation. Our results contribute to the understanding of the morphological structures that allow for sperm storage in viviparous osteichthyes and suggest a positive relationship between superfetation and the capacity of females to store sperm.
... In addition to being highly matrotrophic, H. formosa exhibits a high level of superfetation, with females simultaneously carrying several broods of young at different stages of development (Travis et al. 1987). The maximum level of superfetation reported for H. formosa is nine broods (Scrimshaw 1944;Reznick and Miles 1989) however females typically carry two to five broods (Travis et al. 1987;Leips and Travis 1999;Schrader and Travis 2009). Finally, crosses between populations with large differences in offspring size at birth demonstrate that embryos are able to influence the level of maternal investment they receive during development (Schrader and Travis 2009). ...
... Average Scrimshaw 1944;Snelson et al. 1986;Reznick et al. 1996;Leips and Travis 1999;Schrader and Travis 2009 Reznick et al. 2002;Banet and Reznick 2008;Pires et al. 2011 The decline in offspring size with birth order that we observed is consistent with the presence of asymmetric competition between broods of embryos. However, because we fed each pair a constant amount of food throughout the experiment, it is also possible that this pattern reflects increasing resource limitation. ...
Data Archived: Dryad doi:10.5061/dryad.ng20q Asymmetric sibling competition arises when siblings with different competitive abilities share a limited resource. Such competition occurs in species with postnatal parental care and may also occur when mothers provision embryos between fertilization and birth (matrotrophy). We hypothesized that the combination of matrotrophy and the simultaneous provisioning of embryos in different stages of development (superfetation) leads to asymmetric competition between sibling embryos. Moreover, we expect the intensity of this competition to increase with the level of superfetation as high levels of superfetation result in greater temporal overlap between broods. This hypothesis predicts that offspring from early broods, which predominantly compete with less-developed siblings, will be larger at birth than offspring from later broods, which experience competition from more and less-developed siblings. Data on offspring size at birth from two populations of the highly matrotrophic fish, Heterandria formosa, and similar studies of poeciliid fish spanning a range of life histories are consistent with our hypothesis. Together these results suggest that sibling competition is a direct consequence of the evolution of matrotrophy and superfetation in poeciliid fish. K E Y W O R D S : Heterandria formosa, size at birth, sibling competition, placenta. Sibling competition for parentally supplied resources is a conspic-uous aspect of family life in many species with parental care. This competition may take the form of nonlethal begging scrambles be-tween dependent young or more dramatically fatal sibling rivalry (reviewed in Mock and Parker 1997). The outcome of sibling competition for parentally supplied resources will often depend on the degree to which siblings differ from one another in their competitive abilities. For example, in many birds asynchronous hatching results in initial size disparities among nestlings. These disparities determine the outcome of sibling competition (Magrath 1990; Mock and Parker 1997; Stoleson and Beissinger 1997) with earlier hatched or "core" nestlings outcompeting their later hatched "marginal" siblings (Mock and Forbes 1995). As a consequence, core nestlings typically have higher growth rates and are more likely to survive the nestling period than marginal nestlings (Spear and Nur 1994; Stoleson and Beissinger 1997). Theory predicts that under this type of asymmetric competition (Forbes and Glassey 2000) offspring that hatch earlier should take a disproportionate share of parentally supplied resources at the expense of their siblings that hatch later (Parker et al. 1989). Moreover, differences in growth and survival prospects between core and marginal offspring are expected to increase with a de-scending brood rank (Parker et al. 1989). Sibling competition has been studied most thoroughly in species with postnatal parental care such as birds (reviewed in Mock and Parker 1997) and some insects (e.g., Smiseth et al. 2007). Sibling competition may also be important in species that provision broods of young between fertilization and birth (Ahnesjo 1996; Mock and Parker 1997; Curley et al. 2004). This mode of reproduction is often referred to as matrotrophy and 2 7 2 C 2011 The Author(s). Evolution C 2011 The Society for the Study of Evolution. Evolution 66-1: 272–279
... In order to interpret differences in reproductive investment from the perspective of the altricial-precocial life-history theory, there must be a relationship between reproductive investment and 'quality' of the offspring (Scrimshaw 1944, Blaxter 1988, Flegler-Balon 1989. We found that offspring of L. parva exhausted their yolk supplies at smaller body sizes and at less advanced morphological states, compared to the offspring of L. goodei. ...
... Together, these observations support the idea that the initial formation of the embryo is controlled more by factors associated with the cytoplasm than the yolk mass (cf. Scrimshaw 1944). ...
Important differences were observed in the early ontogenies ofLucania parva andLucania goodei. These differences can be explained in terms of the altricial-precocial model of speciation.Lucania parva can be recognized as an altricial form that produces many eggs with relatively little yolk investment, compared to the more precocialL. goodei. Many of the differences observed in embryo, larva and juvenile specimens appear to be related to these differences in gamete investment. Accelerated developmental rates in the precocial form suggest that paedomorphosis is an important proximate mechanism in the bifurcation of alternative life-history styles in this genus. Some morphological characteristics, such as vitelline circulation and body shape, may be transformations associated with the particular environmental conditions in which the animals must develop and survive. Our observations suggest that these two species in the genusLucania have followed different ontogenic trajectories in response to prevailing environmental conditions.
... Anablepidae and Goodeidae exhibit extreme matrotrophy, increasing in dry mass one thousandfold over embryonic development [21,22]. In contrast, poeciliid embryos receive varying amounts of post-fertilisation nutrition ranging from a decrease in dry mass of 57% to an increase of 625% [9,25,26]. Patrotrophy has evolved at least once in teleosts in the Syngnathidae family [3], but has not yet been studied in other male-brooding teleosts, for example, the forehead-brooding Kurtidae [27], or mouth-brooding Apogonidae [27] and Ariidae [28]. ...
The source of embryonic nutrition for development varies across teleost fishes. A parentotrophy index (ratio of neonate: ovulated egg dry mass) is often used to determine provisioning strategy, but the methodologies used vary across studies. The variation in source and preservation of tissue, staging of embryos, and estimation approach impedes our ability to discern between methodological and biological differences in parentotrophy indices inter- and intra-specifically. The threshold value used to distinguish between lecithotrophy and parentotrophy (0.6–1) differs considerably across studies. The lack of a standardised approach in definition and application of parentotrophy indices has contributed to inconsistent classifications of provisioning strategy. Consistency in both methodology used to obtain a parentotrophy index, and in the classification of provisioning strategy using a threshold value are essential to reliably distinguish between provisioning strategies in teleosts. We discuss alternative methods for determining parentotrophy and suggest consistent standards for obtaining and interpreting parentotrophy indices.
... Superfetation, the ability of females to simultaneously carry multiple broods of embryos at different developmental stages (Scrimshaw, 1944a), is another reproductive strategy that occurs in some genera of Poeciliidae such as Heterandria and Poeciliopsis (Scrimshaw, 1944b;Thibault & Schultz, 1978), whereas it is absent in other poeciliid genera such as Brachyrhaphis and Gambusia (Johnson & Belk, 2001;Riesch, Martin & Langerhans, 2013). The degree of superfetation (i.e. the number of simultaneous broods that females bear) also varies substantially among species as well as among populations within species Z uñiga-Vega, Reznick & Johnson, 2007;Fr ıas-Alvarez et al., 2014;Z uñiga-Vega, Olivera-Tlahuel & Molina-Moctezuma, 2017). ...
In viviparous fishes, females of species that exhibit matrotrophy (post‐fertilization maternal provisioning to developing embryos) and superfetation (ability of females to bear simultaneously multiple broods of embryos at distinct developmental stages) increase less in mass and volume during pregnancy than females of species that lack these traits. Such a reduction in reproductive allocation may provide greater benefits to young and small females for two reasons. First, they could devote energy and resources to both growth and reproduction. Second, they could compensate for the space restrictions that are inherent to a small body size because both superfetation and matrotrophy maximize fecundity for any given ovarian volume. In this study, we test the hypothesis that both matrotrophy and superfetation will decrease over female reproductive lifespan (i.e. as they grow larger). We examined reproductive females from 77 populations of 13 species of the family Poeciliidae. Remarkably, we found support for the matrotrophy prediction in only three populations. As expected, in these populations, small females were more matrotrophic than larger females, which in turn exhibited a predominantly lecithotrophic strategy. In one population, we found the opposite pattern—the degree of matrotrophy actually increased in larger females. With respect to superfetation, none of the populations showed a pattern consistent with our prediction. In fact, in five populations the pattern was opposite to our expectation—larger females produced more simultaneous broods than smaller females. Our findings reveal that the degree of matrotrophy and superfetation can vary throughout the adult lifespans of poeciliid fishes, but such ontogenetic shifts are not common in natural populations.
... It has been shown that such effects can be severe enough to lead to complete population failure (Nash et al., 2004c;Schoenfuss et al., 2009). While sperm motility may serve as a good indicator of fertilization success for spawning fish (Scrimshaw, 1944), this variable could not be easily used in the research with Heterandria formosa since it's fertilization is internal . These findings demonstrate that the present study's observation of a lower population size for the EE2-exposed populations at the end of the study period could potentially be due to a variety of effects brought about by the EE2. ...
Feminization responses have been observed in some wild populations of fish living in rivers and streams, some of which have been shown to arise as a consequence of exposure to sewage treatment (STP) effluent discharges and the endocrine disrupting chemicals (EDCs) they contain which mimic or antagonize the actions of steroid hormones. The synthetic estrogen, 17α-ethinylestradiol (EE2), commonly used in oral contraceptives, is present in surface waters receiving STP effluents at concentrations ranging from non-detectable to 5 ng/L. Despite extensive evidence that EE2 negatively affects the reproductive health of fishes, relatively little is known about effects at the population level – and especially so for live-bearing fishes. To investigate the potential for such impacts, populations of the least killifish (Heterandria formosa) were exposed to 0 or 5 ng/L EE2. Exposures were started with newborn fish and continued for seven months. Chronic exposure to 5 ng/L EE2 caused significant reductions in population size, in abundances of newborns and males, and in population growth rates. The exposure also resulted in a female-biased sex ratio. However, individuals’ survival rates were not affected. This study showed that chronic exposure to 5 ng/L EE2 negatively affected population dynamics in a live-bearing fish, demonstrating that the levels of EE2 detected near STPs have the potential to impact wild populations of these fish.
... At this size, both sexes may be approaching sexual maturity, but none of the females was obviously gravid. The absence of gravid females was further evidenced by the fact that the first offspring did not appear until approximately two months after this time period, because the gestation period is approximately 35 d [28,29]. Females and males (n ϭ 17 of each sex) were randomly selected from each of the parental populations, and pairs of fish were placed in a plastic bucket (height, 16 cm; radius, 8 cm) within a large, fiberglass tank (2.4 ϫ 1.2 ϫ 0.3 m). ...
Fitness costs constrain the evolution of resistance to environmental stress in populations. We earlier reported on a rapid response to laboratory selection for cadmium resistance in the least killifish (Heterandria formosa). By the sixth generation, the three selection populations were threefold more resistant to cadmium than the control populations. Here, we report the fitness costs and trade-offs associated with this evolution of resistance. In the F3 and F4 generations, the selection populations produced smaller-sized offspring than the control populations. A comprehensive life-history traits study in the F7 generation showed that the selection populations had, on average, an 18% decrease in fecundity. The selection populations also had a smaller brood size, longer time to first reproduction, and shorter female life expectancy than the control populations. Our results strongly suggest that fitness costs and trade-offs were associated with the evolution of resistance to cadmium in the least killifish. The fitness costs and trade-offs may result from maintenance of the underlying resistance mechanisms, leading to changes in resource allocation in the cadmium-adapted fish.
... The embryonic growth is supported by matrotrophy in response to scarce yolk deposited during the oogenesis (Uribe & Grier, 2011). The higher degree of maternal nutrients provision during embryogenesis is estimated through the increment of the dry weight of the embryo at the time of fertilization (0.017 mg) to that at birth (6.8 mg), which represented an enlargement of 39,900% (Scrimshaw, 1944a). Modifications of the follicular layer (e.g., number of microvilli and vesicles) and hypertrophy of the embryonic pericardial sac permit the substantial transference of nutrients and additionally, in species with presence of superfetation, the development of a more complex placenta (Olivera-Tlahuel et al., 2018;Turner, 1940a). ...
Heterandria formosa is a viviparous poeciliid native of the southeastern of United States of America. H. formosa exhibits unique reproductive features as: (a) production of extremely small eggs with scarce quantity of yolk (microlecithal eggs), (b) consequently, a high level of matrotrophy and development of a complex follicular placenta, (c) ovarian sperm storage that allows the continuous fertilization of oocytes and production of offspring and (d) development of high degree of superfetation. The degree of superfetation refers to the number of broods in different simultaneous stages of gestation. Morphological evidence of the degree of superfetation in H. formosa has not been documented. Therefore, and because of the general interest in the complex process of superfetation, the goal of this study is to morphologically define the degree of superfetation of H. formosa through two procedures: (a) histological analysis of entire ovaries in gestation and (b) dissection of visible embryos and the histological analysis of the remaining ovarian tissue. Results indicate that H. formosa can gestate up to seven broods at the same time. Superfetation degree in Heterandria formosa. (a) Five broods of embryos obtained by dissection with dissecting microscope were identified, in stages from optic cup (S6) to very‐late eyed embryo (S10). (b, c) Two histological sections of the remaining ovarian tissue with embryos in stages of blastodisc (S4) and shield/primitive streak (S5), both broods not visible by dissection. Bar = a: 1 mm, b: 200 μm, c: 200 μm.
... Fertilization is internal, and sperm can be stored in the female's ovary for more than 10 months (Constanz 1989;Rosen and Bailey 1963). They have a gestation period of 27 to 35 days (Fraser and Renton 1940;Scrimshaw 1944), and fertilized eggs are retained within the ovary until the embryos are fully developed and large enough to be self-sufficient and free swimming (Rosen and Bailey 1963). Females produce one to ten offspring per brood, and superfetation allows the females to have successive broods with intervals as short as a few days (Cheong et al. 1984;Reznick et al. 1996;Travis et al. 1987). ...
17α-ethinylestradiol (EE2) is a potent synthetic estrogen that is routinely detected in aquatic ecosystems and exhibits estrogenic activity. Acute and chronic toxicity have been described for oviparous and ovoviviparous fish species; however, no information is available on the impacts of EE2 on viviparous, matrotrophic fish despite their ecological importance. The present study investigated the consequences of long-term EE2 exposure in the least killifish (Heterandria formosa). Effects on growth, time-to-sexual maturity, fecundity, and offspring survival were examined in an 8-month, life-cycle experiment. Starting as 0–6-day-old fish, least killifish were continuously exposed to EE2 at nominal concentrations of 0, 5, or 25 ng/L (measured concentrations averaged 0, 4.3, and 21.5 ng/L respectively). In the F0 generation, EE2-exposure did not affect survival but resulted in increased time-to-sexual maturity and a sex-dependent effect on size; female standard length was reduced while male standard length was increased. This caused the ordinarily larger females and smaller males to become more similar in size. Condition factor was reduced for both sexes. Fecundity was reduced by 50% and 75% at 5 and 25 ng/L EE2-exposure respectively. Continued EE2-exposure in the F1 generation resulted in significantly reduced survival. These results suggest that despite their matrotrophic development, these fish experience delayed development and reduced reproductive success from EE2-exposure and that effects appear to intensify in the second generation.
... Fertilization is internal, and sperm can be stored in the female's ovary for more than 10 months (Constanz 1989;Rosen and Bailey 1963). They have a gestation period of 27 to 35 days (Fraser and Renton 1940;Scrimshaw 1944), and fertilized eggs are retained within the ovary until the embryos are fully developed and large enough to be self-sufficient and free swimming (Rosen and Bailey 1963). Females produce one to ten offspring per brood, and superfetation allows the females to have successive broods with intervals as short as a few days (Cheong et al. 1984;Reznick et al. 1996;Travis et al. 1987). ...
The widespread use of the synthetic estrogen 17 α-ethinylestradiol (EE2) has resulted in elevated levels in aquatic environments, where it is known to act as an endocrine disrupting chemical affecting fish and other aquatic organisms. Examining changes in the structure of the fish’ gonads and liver has proven to be an effective approach for assessing these impacts. While changes have been reported for various fish species, it is not clear whether impacts are equally severe in live-bearing fishes. The present study looked at gonadal and liver development in EE2-exposed least killifish (Heterandria formosa), a live-bearing Poeciliid. Exposures to 0, 5, or 25 ng/L EE2 began within six days of birth and continued until fish became sexually mature 12–23 weeks later. Exposure to 5 ng/L EE2 resulted in severe intersex in fish with external male characteristics, a slowdown of spermatogenesis in these intersex fish and a slowdown of oogenesis in the female fish. Moreover, these fish had a variety of liver injuries. Fish exposed to 25 ng/L EE2 exhibited intersex but at a lower frequency than occurred at 5 ng/L. In contrast, liver damage and slowdown of both oogenesis and spermatogenesis exhibited the typical dose-dependence. These findings illustrate the importance of including histological analyses when assessing endocrine disruption in fish, demonstrate that the live-bearing mode of reproduction appears to provide limited protection from the effects of waterborne EE2, and provide further evidence that EE2 has multiple impacts on fish health and reproduction that are severe enough to potentially affect fish populations.
... Anatomical studies of a subset of these species (e.g. Turner, 1937Turner, , 1940Wourms et al., 1988;Grove & Wourms, 1991, 1994Scrimshaw, 1944a;Kwan et al., 2015;Olivera-Tlahuel et al., 2018) reveal that maternal provisioning is via a combination of the maternal follicle and modified embryonic tissues. The embryonic side of the placenta may be either a modified yolk sac or an externalized pericardial membrane (Turner, 1940). ...
We describe the occurence of extensive post-fertilization maternal provisioning (matrotrophy) in fish species in the subgenus Pamphorichthys (genus Poecilia: family Poeciliidae) that represents one of two independent origins of this adaptation in this genus. Matrotrophy is accompanied by a reduction in yolk in eggs at fertilization, a thickened follicle throughout development, and externalization and anterior extension of the embryonic pericardial membrane. These features resemble the anatomical adaptations for placentotrophy described in other members of this family and accompany a substantial increase in dry mass of the embryo during development. Species mean values for the increase in embryo mass range from a low of less than two-fold (Pamphorichthys minor) to greater than 50-fold (Pamphorichthys hasemani). Different populations of Pamphorichthys araguaiensis show a range from less than a two-fold to greater than 16-fold increase in dry mass during development. Such substantial differences in matrotrophy among closely related species and within species make Pamphorichthys a promising group with which to study the adaptive value and the genetic basis of matrotrophy.
... The results obtained in the present study add this subgenus to the list of independent origins of extensive placentotrophy in poeciliid fishes. Other origins are found in H. formosa (Turner, 1940;Scrimshaw, 1944a;Grove & Wourms, 1991;Schrader & Travis, 2005; MI of approximately 40-50) and three clades in the genus Poeciliopsis (Reznick et al., 2002; 13 of 21 species are placentotrophic, with MI values in the range 0.8-117). Placentotrophy is also found in P. caudimaculatus (Arias & Reznick, 2000; MI of approximately 2) and Xenodexia ctenolepis MI of approximately 3-5). ...
Examining the association between trait variation and development is crucial for understanding the evolution of phenotypic differences. Male guppy ornamental caudal fin coloration is one trait that shows a striking degree of variation within and between guppy populations. Males initially have no caudal fin coloration, then gradually develop it as they reach sexual maturity. For males, there is a trade‐off between female preference for caudal fin coloration and increased visibility to predators. This trade‐off may reach unique endpoints in males from different predation regimes. Caudal fin coloration includes black melanin, orange/yellow pteridines or carotenoids, and shimmering iridescence. This study examined the phenotypic trajectory and genetics associated with color development. We found that black coloration always developed first, followed by orange/yellow, then iridescence. The ordering and timing of color appearance was the same regardless of predation regime. The increased expression of melanin synthesis genes correlated well with the visual appearance of black coloration, but there was no correlation between carotenoids or pteridine synthesis gene expression and the appearance of orange/yellow. The lack of orange/yellow coloration in earlier male caudal fin developmental stages may be due to reduced expression of genes underlying the development of orange/yellow xanthophores.
... Specialized embryonic absorptive structures have been described in other viviparous teleosts. The trophotaeniae in Goodeidae, Zoarcidae and ophidioid fishes (Turner 1940aj Bretschneider & De Wit 1947Mendoza 1956Mendoza , 1958Mendoza , 1972Wourms & Cohen 1975), the extended pericardial and yolk sac areas in Poeciliidae and Anablepidae (Turner 1938Turner , 1940bScrimshaw 1944) and in most cases a hypertrophied embryonic gut plays a role in nutrient absorption (Igarashi 1962;Veith 1980). Some of these specialized absorptive structures have been shown to possess microvilli which increase the surface area available for absorption of nutrients. ...
Embryos of Clinus dorsalis absorb nutrients from the embiyotrophe, secreted by the follicular epithelium. Autoradiographic studies revealed that the principal areas of nutrient absorption are the embryonic gut and epidermis. A histological and electron microscopic study of embryonic structure revealed an extensively hypertrophied gut with numerous flngerlike villi projecting into the gut lumen. A brushborder of microvilli is, furthermore, characteristic of the columnar gut epithelium. Epidermal surface area is increased apically on individual epidermal cells, particularly on the ventral pericardial surface. Micro ridges further increase epidermal surface area. Epidermal surface area is reduced and a mucous layer is secreted prior to parturition.Embrio's van Clinus dorsalis absorbeer voedsel vanuit die embriotroof wat deur die follikuldre epiteel gesekreteer word. Outoradiograflese studies het getoon dat die belangrlkste geblede vir voedselabsorpsie die embrioniese spysverteringskanaal en epidermis is. 'n Histologiese en elektronmlkroskopiese ontleding van hlerdie embrioniese strukture het getoon dat die spysverteringskanaal gehipertrofeer is en dat talle vingeragtige villi in die S.V.K.- lumen voorkom. Die sllinderepiteel van die S.V.K. is ook 2 voorsien met 'n goed ontwikkkelde borselrant bestaande uit mikrovilli. Die epldermale oppervlakte van die embrio's word vergroot deur bulte wat gevorm word deur die apikale 5 oppervlakte van indiwiduele epidermale selle veral op die ventrale perikardiale oppervlakte van die embrio's. Mikrorlwwe vergroot die epldermale oppervlakte verder.Voor geboorte word die epidermale oppervlakte verminder en 'n slymlaag word gesekreteer.
... Matrophy index (I M ) was calculated as the estimated mass of a fully developed embryo, as predicted by this regression, divided by the estimated mass of the egg at fertilization, which is the y-intercept of this regression (Regus et al., 2013). In previous studies of lecithotrophic poeciliids (little or no maternal provisioning), the relationship between dry mass and stage of development is linear with a negative slope, indicating c. 30-40% loss in embryo dry mass during development (Turner, 1937(Turner, , 1940Scrimshaw, 1944;Thibault & Schultz, 1978;Reznick & Endler, 1982;Mateos et al., 2002). In contrast, matrotrophic species produce a positive regression slope, suggesting that embryo masses increase during development (Reznick et al., 2002). ...
This study presents life-history descriptions for 12 species in the subgenus Limia, which are endemic to the Greater Antilles. All species in this study lack evidence of superfoetation, producing a single brood of offspring before developing subsequent broods. Interbrood intervals (number of days between parturition events) are also consistent with intervals of species that lack superfoetation. Maternal provisioning, characterized by matrotrophy index, is <1.0 for all species of Limia. This is consistent with species that provide little or no maternal provisioning to developing embryos after ovum fertilization (lecithotrophic). Four species exhibit potentially bi-modal size distributions of mature males. Work on other poeciliids suggests that such bimodal distributions can be caused by genetic polymorphisms in some species. Principle component analyses revealed an axis of interspecific variation in life histories that separated species with small size at maturity and the production of many, small offspring from those with large size at maturity and that produce few, large offspring. This pattern of life-history diversity occurs in many other groups of organisms.
© 2015 The Fisheries Society of the British Isles.
... The occurrence of aborted broods and of broods containing dead offspring may both reflect embryo mortality during development. The same mortality occurring at an earlier stage, could result in resorption of embryonal tissue and consequently smaller broods (Meffe and Vrijenhoek, 1981;Turner, 1947;Scrimshaw, 1944). Similarly, early broods are more likely to occur too early to allow for full and normal development, and an early brood could set the stage for a longer interval till the next birth. ...
We investigated the reproductive effects of a 10-day maternal metal exposure in the live-bearing western mosquitofish. We exposed gravid females to 0.15µM copper or cadmium and monitored reproduction-related variables over the subsequent 8-month breeding season. Females gave birth to 1-5 broods, a number not affected by the exposure. Their first brood's size was reduced following exposure to either metal, while this effect was still evident for the second brood of copper-exposed females. Metal-exposed females also had more premature births, abortions, and broods containing dead offspring; these last two effects were still evident in second broods. The time-till-first-birth was reduced while the time-interval between first and second brood was increased in cadmium-exposed females, but not in copper-exposed ones. This study demonstrated that short-term metal exposure affects a variety of reproductive measures and that effects can still occur in broods that developed well after the end of the females' exposure.
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... Females also exhibit superfetation, simultaneously carrying multiple broods of offspring at different stages of development. The gestation period for this species is 27-35 days (Fraser and Renton 1940;Scrimshaw 1944) and superfetation allows females to give birth continuously throughout a breeding season, with the interval between successive broods being as short as a few days (Cheong et al. 1984;Travis et al. 1987;Reznick et al. 1996). Extreme matrotrophy and superfetation, in combination, provide the opportunity for females to adjust their investment in offspring continuously in response to environmental circumstances. ...
Given a trade-off between offspring size and number and an advantage to large size in competition, theory predicts that the offspring size that maximizes maternal fitness will vary with the level of competition that offspring experience. Where the strength of competition varies, selection should favor females that can adjust their offspring size to match the offspring's expected competitive environment. We looked for such phenotypically plastic maternal effects in the least killifish, Heterandria formosa, a livebearing, matrotrophic species. Long-term field observations on this species have revealed that some populations experience relatively constant, low densities, whereas other populations experience more variable, higher densities. We compared sizes of offspring born to females exposed during brood development to either low or high experimental densities, keeping the per capita food ration constant. We examined plastic responses to density for females from one population that experiences high and variable densities and another that experiences low and less-variable densities. We found that, as predicted, female H. formosa produced larger offspring at the higher density. Unexpectedly, we found similar patterns of plasticity in response to density for females from both populations, suggesting that this response is evolutionarily conserved in this species. K E Y W O R D S : Competition, life-history strategies, maternal effects, optimal offspring size, phenotypic plasticity. Environmental conditions experienced by offspring during pre-and postnatal development can have dramatic effects on their fitness (e.g., Clutton-Brock 1991; Mousseau and Fox 1998; Holbrook and Schal 2004). An important source of these effects is the maternal environment; stressful conditions experienced by the female parent can reduce offspring fitness (McCormick 1998; Jann and Ward 1999; Naguib et al. 2006) but, in certain cases, All authors contributed equally in this article. mothers respond to environmental challenges by manipulating the phenotype of individual offspring to enhance their fitness in that environment. These adaptive maternal effects include adjust-ments of nutrient provisioning, hormones (Benton et al. 2005; Meylan and Clobert 2005), and agents that enhance resistance to disease (Spitzer 2004). The initial size of free-living offspring has been a focal trait for studies of adaptive maternal effects because, in a broad range of taxa, the environment experienced by the dam affects size of 1 3 4 1
... The duplication of this result in another ovoviviparous fish lends strength to this interpretation. It remains to be seen if "viviparous" organisms (e.g., the poeciliids Heterandria formosa [Scrimshaw 1944] or Poeciliopses turneri [Thibault and Schultz 1978]), in which newborn offspring can be more than 10 times as heavy as ova at fertilization, display a paternal effect which is not delayed a generation in its expression, as was predicted earlier. Arnold (1980) may have observed such a paternal affect when he hybridized two populations of the viviparous garter snake Thamnophis elegans which differed substantially in offspring weight. ...
Provides a test for the 'grandfather effect' whereby, although the paternal (P1) genome makes no contribution to F1 offspring size, because it contributes to the F1 female genotype, it helps to determine size of F2 offspring. This delayed inheritance is associated with ovovivipary. -P.J.Jarvis
... Superfetation is a condition in which two or more broods of embryos of different ontogenetic stages simultaneously develop within the ovary. Extreme degrees of this condition are achieved in Poeciliopsis prolifica with five broods of embryos (Thibault and Schultz, 1978) and in Heterandria formosa with up to nine broods (Turner, 1937(Turner, , 1947Scrimshaw, 19446). Veith (19796) reported up to twelve broods in the clinid, Clinus superciliosus. ...
SYNOPSIS. Viviparity in the vertebrate line first makes its evolutionary appearance among fishes. It has independently evolved in a number of divergent piscine lineages. The 54 families of extant fishes that bear living young include 40 families of chondrichthyans (sharks and rays), one montypic family of coelacanths (Latimeria), and 13 families of teleosts. There is fossil evidence for viviparity in holocephalans and chondrosteans. Viviparity predominates among sharks and rays (40 families, 99 genera, 420 species) but is less widespread among teleosts (13 families, 122 genera, 510 species). Following an historical introduction, the organization of the female reproductive system, sites of gestation, developmental sequences and superfetation are considered. The evolution of viviparity establishes specialized maternal-fetal relationships, viz., 1) developmental, 2) morphological, 3) trophic, 4) osmoregulatory, 5) respiratory, 6) endocrinological, and 7) immunological. While the latter four categories are briefly noted the major emphasis is on the trophic relationship and its morphological and developmental basis. First, a general overview is presented and then the maternal-fetal trophic relationships in each of the major groups of fishes are systematically reviewed. Pertinent anatomical, histological, ultrastructural, developmental, physiological, and biochemical studies are considered. Viviparous fishes are either lecithotrophic, i.e., exclusively yolk dependent, or matrotrophic, i.e., in receipt of a continuous supply of maternal nutrients during gestation. Nutrient transfer is accomplished by 1) oophagy and adelphophagy, 2) placental analogues, and 3) the yolk sac placenta. Placental analogues include: external epithelial absorptive surfaces, e.g., skin, fins, gills; trophonemata, modifications of the uterine epithelia for the secretion of histotrophe or "uterine milk"; branchial placentae, close apposition between gill epithelia and either uterine or ovarian epithelial villi; the yolk sac; pericardial amnion and chorion; follicular pseudoplacenta, close apposition between follicle cells and embryonic absorptive epithelia; hypertrophied gut; and trophotaeniae, external rosette or ribbon-like projections of the embryonic gut. Among chondrichthyans, the yolk sac placenta (840-1,050%), trophonematal secretion and embryonic absorbtion of histotrophe (1,680-4,900%) and oophagy and adelphophagy (1.2 × 106%) are the most efficient methods of nutrient transfer. Among teleosts, the follicular pseudoplacenta (1,800-3,900%), trophotaeniae (8,400%) and absorption of ovarian histotrophe through surface epithelia and a hypertrophied gut (1,100-34,000%) are the most efficient. These values stand in contrast to the 30%40% loss of dry weight characteristic of oviparous fishes and viviparous lecithotrophes.
... Matrotrophy is present in at least 11 lineages within the family (Figure 2; not all origins are shown here), including H. formosa (Scrimshaw 1944a ...
The placenta is a complex organ that mediates all physiological and endocrine interactions between mother and developing embryos. Placentas have evolved throughout the animal kingdom, but little is known about how or why the placenta evolved. We review hypotheses about the evolution of placentation and examine empirical evidence in support for these hypotheses by drawing on insights from the fish family Poeciliidae. The placenta evolved multiple times within this family, and there is a remarkable diversity in its form and function among closely related species, thus providing us with ideal material for studying its evolution. Current hypotheses fall into two categories: adaptive hypotheses, which propose that the placenta evolved as an adaptation to environmental pressures, and conflict hypotheses, which posit that the placenta evolved as a result of antagonistic coevolution. These hypotheses are not mutually exclusive. Each may have played a role at different stages of the evolutionary process.
... The results obtained in the present study add this subgenus to the list of independent origins of extensive placentotrophy in poeciliid fishes. Other origins are found in H. formosa (Turner, 1940; Scrimshaw, 1944a; Grove & Wourms, 1991; Schrader & Travis, 2005; MI of approximately 40–50) and three clades in the genus Poeciliopsis (Reznick et al., 2002; 13 of 21 species are placentotrophic, with MI values in the range 0.8–117). Placentotrophy is also found in P. caudimaculatus (Arias & Reznick, 2000; MI of approximately 2) and Xenodexia ctenolepis (; MI of approximately 3–5). ...
Complex adaptations are often found in nature, although our ability to discern how and why such traits evolved is limited because their origin occurred in the distant past and the details of their evolution have been lost through extinction (e.g. all placental mammals inherited their placentas from a single common ancestor that lived over 100 Mya). In poeciliid fishes, placentas have evolved independently multiple times and portions of the path to the evolution of complexity can be found in living species. In the present study, we describe the life histories of six species within the genus Poecilia that includes the subgenera Micropoecilia and Acanthophacelus (the guppy; Poecilia reticulata). We demonstrate that extensive placentotrophy and superfetation, the ability to simultaneously carry more than one developing brood, have evolved within this clade. These fish represent the third clade in which we have discovered the independent origin of a placenta that also includes close relatives that lack a placenta. We discuss possible adaptive advantages of the joint evolution of extensive placentation and superfetation in these fishes. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 784–796.
... This allows for short intervals between successive broods (from 7–21 d; Travis et al. 1987, Leips 1997) and results in several overlapping generations per breeding season. Females are matrotrophic; embryos are nourished by direct provisioning of nutrients from the female (Fraser and Renton 1940, Scrimshaw 1944), enabling changes in resource availability to be translated directly to developing offspring. Overview of experiment We followed the numerical dynamics and life history trait expression of H. formosa from replicated experimental populations composed of one of five different JEFF LEIPS ET AL. ...
When natural populations differ in density or in the dynamic fluctuations of population size, some of those differences may result from their different ecological con-ditions, and some may originate from genetically based differences in life history expres-sion. Natural populations of the live-bearing poeciliid fish, Heterandria formosa, vary considerably in their population dynamics, with densities that differ between populations by as much as sevenfold. This system offers an excellent opportunity to explore the potential role of genetically based differences in life history expression in creating different dynamic patterns in a common environment. We created five different genetic stocks of H. formosa by carrying out a series of crosses using fish from two North Florida populations (the Wacissa River and Trout Pond) and used them to initiate replicate experimental populations in artificial ponds. The five stocks consisted of two ''controls,'' which were pure Wacissa River and Trout Pond stocks, and three types of hybrid stocks. The hybrid stocks differed in a regular way in the proportion of genes from one population or the other. The crossing scheme was designed so that each hybrid stock would have the same proportion of het-erozygous (or ''heterodemic'') loci but would differ in the proportion and/or identity of homozygous (or ''homodemic'') loci from the Wacissa River and Trout Pond populations. These populations were chosen because a previous study had found that population densities in the Wacissa River greatly exceeded those of Trout Pond and exhibited a higher range of population fluctuation during the breeding season. We addressed four questions in this experiment: (1) Are there genetically based differences in life history traits of fish from the two populations? (2) If so, do differences in life history expression produce differences in population dynamics in a common environment? (3) Which traits have the greatest influence on population dynamics? (4) How do changes in density affect the phenotypes of individual traits that govern the rates of birth and death in a population? We followed experimental populations of the five genetic stocks from their initiation at low density through 4–6 generations of population growth and decline. The mean offspring size differed among stocks by as much as 50%. At low densities, offspring size exhibited a trade-off with brood size: Trout Pond alleles were associated with more, smaller offspring. At higher densities, offspring sizes were similar among stocks, and the trade-off with offspring number was not evident. Stocks differed in realized population growth rate by as much as 70%; the rank order differences among stocks with respect to population growth rate appeared to match the genetic relatedness among stocks based on the expected percentage of Trout Pond alleles. Differences in population growth rate appeared to be due to differences in brood size among stocks at low density. Stocks did not differ in the equilibrium population size, which indicated the absence of a trade-off between population growth rate and carrying capacity in this environment. Adult survival and recruitment of juveniles into the adult population both declined linearly with increasing density; and stocks did not generally differ in those rates after the effects of density had been taken into account. The stocks differed in their response to the depressant effects of density on life history trait expression. The offspring size of the pure Wacissa River stock was much more sensitive to density than was the offspring size of the pure Trout Pond stock. However, the brood sizes of the Wacissa River stock were reduced much less than those of the Trout Pond stock when exposed to the same high density. These results suggest that life history distinctions among populations, both in the mean values and plasticity of traits, play a role in creating different dynamics. We discuss the ways in which phenotypic plasticity in reproductive traits potentially acts as a mechanism to stabilize population dynamics in this species.
... In order to interpret differences in reproductive investment from the perspective of the altricialprecocial life-history model, there must be a relationship between reproductive investment and 'quality' of the offspring (Scrimshaw 1944, Blaxter 1988, Flegler-Balon 1989. Crawford & Balon (1994c) found that offspring of L. parva exhausted their yolk supplies at smaller body sizes and at less advanced morphological states, compared to the offspring of L. goodei. ...
Egg size alone is a poor and misleading variable in life-history studies. A mathematical technique for estimating yolk and blastodisc volume ratios in fishes, a much more meaningful character, is generated from first principles. The technique is demonstrated with an example of early ontogeny in fishes of the genus Lucania (Pisces: Cyprinodontidae). Wild, adult rainwater killifish, Lucania parva, and bluefin killifish, L. goodei, were collected in Florida and transported to the laboratory, where offspring were reared under controlled conditions. Offspring were sampled at the onset of cleavage, for simple measurements of yolk and blastodisc morphology. Application of mathematical equations allowed estimates of yolk and blastodisc volumes in the two species. No significant differences were found in clutch size, blastodisc volume, or egg density; however, significant differences existed in the absolute yolk investments, and blastodisc:yolk volume ratios. These differences in reproductive investment within the genus Lucania are interpreted by the altricial-precocial life-history model as a possible causal mechanism in the evolution of species within this genus. The mathematical equations presented in this study enabled us to partition reproductive investment into components that are more biologically meaningful than simple egg size.
When natural populations differ in density or in the dynamic fluctuations of population size, some of those differences may result from their different ecological conditions, and some may originate from genetically based differences in life history expression. Natural populations of the live-bearing poeciliid fish, Heterandria formosa, vary considerably in their population dynamics, with densities that differ between populations by as much as sevenfold. This system offers an excellent opportunity to explore the potential role of genetically based differences in life history expression in creating different dynamic patterns in a common environment. We created five different genetic stocks of H. formosa by carrying out a series of crosses using fish from two North Florida populations (the Wacissa River and Trout Pond) and used them to initiate replicate experimental populations in artificial ponds. The five stocks consisted of two “controls,” which were pure Wacissa River and Trout Pond stocks, and three ty...
The fishes, like all the other vertebrates, reproduce sexually. This chapter describes embryology, as well as morphology that is essential to understand the features of the comparative physiology of the reproductive system of fishes. In majority of species, eggs and spermatozoa are formed in separate individuals and the gametes are expelled into the surrounding water where fertilization takes place and is followed by the development of a new generation. The modes of reproduction are unusual and most of the 20,000 or more known species of fish have male and female organs in separate individuals. Sexual activities are normally followed by the prompt fertilization of eggs, but sometimes sperms are stored in the female for prolonged periods prior to fertilization. Sometimes development occurs, but hatching is delayed during adverse environmental condition. Many specializations associated with reproduction in fishes are discussed in this chapter.
This chapter discusses the maternal–embryonic relationship in viviparous fishes. Viviparity is a highly successful mode of reproduction that has evolved independently many times and with many variations in widely separated taxonomic groups. It occurs in all classes of vertebrates, except birds, and among many different groups of invertebrates. Initial steps in the evolution of viviparity involved a shift from external to internal fertilization and the retention of fertilized eggs in the female reproductive system. The osmoregulation of early embryos can be accomplished more efficiently and with less expenditure of embryonic energy in a maternally controlled uterine environment, but as development progresses to term, the embryos presumably acquire an increasing degree of osmoregulatory independence. Available evidence suggests that maternal regulation of the osmotic and chemical environment of the embryo also confers a selective advantage on viviparous teleosts. The uterine wall of most viviparous elasmobranchs and the coelocanth both delimits and defines the embryonic environment. The most spectacular maternal specializations for uterine gestation involve the uterine wall and involve (1) the amplification of the surface area in the form of folds, villi, or trophonemata; (2) the production of histotrophe or uterine milk’ (3) the compartmentalization of embryos; and (4) the development of placental attachment sites.
Reproductive Biology of Teleost Fishes is the first integrated review of the reproductive biology of the bony fishes, which are the most species-rich and diversified group of vertebrates. Teleosts display remarkable variation in their modes of reproduction, and this volume is intended to provide a framework for understanding the remarkable reproductive diversity of this group. It describes their reproductive biology using, wherever possible, phylogenetic analyses and life-history theory as a means to interpret the information. The book addresses the genetic, physiological, behavioural, ecological, evolutionary and applied aspects of teleost reproduction in a comparative framework that emphasises the adaptive basis of reproductive diversity. Reproductive Biology of Teleost Fishes provides a comprehensive synthesis of fish reproduction that will be of great interest to life scientists, particularly ecologists, evolutionary biologists, physiologists and advanced undergraduates, postgraduates and research workers requiring a comprehensive overview of fish reproduction. The book is suitable for courses in fish biology and ecology, reproductive physiology and reproductive genetics. It also addresses applied questions and will be of value for courses on fisheries science and aquaculture. Libraries in all universities and research establishments where biological sciences, fisheries science and aquaculture are studied and taught should have several copies of this important book on their shelves.
Studies of the Gila topminnow, Poeciliopsis occidentalis, indicate that onset of reproduction, proportion of reproducing @V @V, and numbers of embryos carried by @V @V are influenced by H"2) temperature, photoperiod, food, and predation. Water temperature and photoperiod act upon the fishes regardless of population density, whereas, nutrition influences and predation are proportionate to population density. Therefore, density dependent and density independent factors operate to regulate reproduction and neither is mutually exclusive.
Within the family Poeciliidae, a wide range of adaptations accompanying viviparity has evolved. The reproductive mechanisms of five representative species were examined and related to the habitats in which they are employed. Poecilia reticulata, the guppy, represents the majority of poeciliids which have a single stage of embryos in the ovary at a time. Most of the nutrients are prepack-aged in the eggs before fertilization; no specialized placental adaptations have evolved. The major variable among species utilizing this mechanism is in the yolk loading time; some eggs are mature and ready to be fertilized immediately after the birth of a clutch of embryos, others take a week or more. The mechanism may be thought of as a generalist-type, being employed throughout the range of poeciliids and in all varieties of habitats. Poeciliopsis monacha has embryos of two different ages occurring simultaneously in the ovary. Its large eggs provide the embryo's entire nutrient supply. Mature embryos weigh 47% less than mature eggs. This species lives in a harsh, montane environment with an unpredictable food supply; its reproductive mechanism is well suited to fluctuating resources. When conditions are favorable, a large clutch of eggs is loaded, but if food is in short supply, clutch sizes are small or only one stage is produced. During starvation conditions, no eggs are produced; but, with restoration of food supply, reproduction resumes quickly. Poeciliopsis lucida has medium-sized eggs and three stages of embryos. At birth, young weigh slightly more than mature ova. This weight gain plus the energy utilized for embryonic metabolism constitutes a significant maternal contribution during development. P. lucida is wide-spread in the three rivers that comprise its range but it does not enter the depauperate rocky arroyos occupied by P. monacha. P. lucida requires a stable food supply characteristic of the fertile and productive downstream regions. Poeciliopsis prolifica carries as many as five stages of embryos which are born at short brood intervals of two to eight days. Ova sizes are small and embryos receive almost all of their nutrients through a placenta. P. prolifica lives in a rich environment where food resources are stable. It is the smallest species in the genus and it produces the smallest young, yet its habitat seems precarious. Living on the steep slope between deep and shallow water it is wedged between deep and shallow water competitors, having to cope with large deep water fish predators as well. Poeciliopsis turneri is the largest of the five species studied and occupies a habitat somewhat unusual for poeciliids. Three stages of embryos are present in the ovary but brood sizes are usually small (ave. 3.6). The ova are small yet the mature embryos are large, weighing almost 19 times more than the ova. Brood sizes in neither P. prolifica nor P. turneri become larger as female size increases. P. turneri is adapted to life in deep swift water where large adults, large offspring and streamlining are important. The other four species can risk the swollen pregnant-look typical of poeciliids, whereas P. turneri cannot. Superfetation (multiple stages of embryos) is advantageous in that it avoids the surge of energy required to load a single large clutch of eggs. The energy for reproduction is sequentially divided among two to five small clutches. Reduction of ova size increases the space available for more stages of embryos. Although embryos with small yolk supplies place a nutrient drain directly on the mother, surges in demand are avoided since embryonic stages enter the growth phase at different times. A continuous food supply to the female is essential; otherwise, embryos will die and the reproductive effort to that point is lost.
Size at birth strongly affected offspring survival but was not correlated with age or with dry weight at maturity. The month in which the fish were born had a significant effect on an age at maturity, possibly caused by an aspect of the environment such as minor temperature changes. Number of offspring in the 1st brood was negatively correlated with the remaining life span of the female. Although number of offspring in a brood was unrelated to average weight of the offspring in that brood, it was negatively correlated with offspring weight in subsequent broods, possibly caused by the energetics of superfetation. In varying the number of offspring in broods and thereby influencing the weight of future offspring, females could display large variation in offspring size at birth.-from Author
The frequency of litter overlap, the simultaneous presence of two litters at different stages of development within a single female, varies among populations of Gambusia hubbsi in different habitats on Andros, Bahamas. In freshwater bluehole and shallow water populations, less than 2% of the females carried two litters, independent of the difference in developmental stage between the litters. In well field populations, 2% of the females carried two litters composed of immature and mature oocytes, whereas 10% carried developing oocytes and late stage embryos, and 16% carried mature oocytes (or older) and late stage embryos. Among females from populations that we introduced into unoccupied well fields 2% carried two litters composed of immature and mature oocytes, about 14% carried developing oocytes and late stage embryos, and less than 6% carried mature oocytes (or older) and late stage embryos. When two litters composed developing oocytes and late stage embryos were present, the two litters were of equal size, and the total number of offspring was 1.5 times larger than expected on the basis of female body length. When two litters composed mature oocytes (or older stages) and late stage embryos were present, the two litters were also of equal size, and the total number of offspring was as expected on the basis of female body length. Litter overlap was independent of female size. A comparison of the consequences of litter overlap for strictly lecithotrophic and strictly matrotrophic modes of reproduction with the patterns of litter overlap observed in G. hubbsi, suggests that litter overlap in G. hubbsi reduces the cost of reproduction, but does not increase the rate of offspring production.
Oogonial proliferation in fishes is an essential reproductive strategy to generate new ovarian follicles and is the basis for unlimited oogenesis. The reproductive cycle in viviparous teleosts, besides oogenesis, involves development of embryos inside the ovary, that is, intraovarian gestation. Oogonia are located in the germinal epithelium of the ovary. The germinal epithelium is the surface of ovarian lamellae and, therefore, borders the ovarian lumen. However, activity and seasonality of the germinal epithelium have not been described in any viviparous teleost species regarding oogonial proliferation and folliculogenesis. The goal of this study is to identify the histological features of oogonial proliferation and folliculogenesis during the reproductive cycle of the viviparous goodeid Ilyodon whitei. Ovaries during nongestation and early and late gestation were analyzed. Oogonial proliferation and folliculogenesis in I. whitei, where intraovarian gestation follows the maturation and fertilization of oocytes, do not correspond to the late oogenesis, as was observed in oviparous species, but correspond to late gestation. This observation offers an example of ovarian physiology correlated with viviparous reproduction and provides elements for understanding the regulation of the initiation of processes that ultimately result in the origin of the next generation. These processes include oogonia proliferation and development of the next batch of germ cells into the complex process of intraovarian gestation. J. Morphol., 2014. © 2014 Wiley Periodicals, Inc.
1. No differences could be established in the embryonic development of the lordotic and normal Lebistes.2. The water content of developing embryos increases during gestation, but the dry and fat-free dry weights remain constant as does the protein concentration.3. The calcium concentration, associated with calcification of osseous tissue, increases markedly during the last week of gestation while the phosphorus concentration increases only slightly during the entire brood interval.
Fluorescent microspheres and confocal microscopy were used to assess matrotrophic transfer in livebearing poeciliid fishes. High levels of transfer occurred in an obligate matrotroph, Heterandria formosa, whereas low levels occurred in a proposed lecithotroph, Poecilia reticulata. Gambusia affinis and Gambusia geiseri, proposed facultative matrotrophs, exhibited variable transfer within each brood.
1.1. The osmolarity and pH of the follicular fluid was determined and analyses of total glucose, total lipids, total proteins, amino acids, urea, sodium and potassium carried out.2.2. The mean osmolarity of the follicular fluid was found to be 325 mOsm/kg and the mean pH was 7.9.3.3. The embryotrophe was rich in lipids (1092.39 mg/100 ml) and amino acids with the amino acid concentration exceeding normal values for human plasma.
In the four-eyed fish, Anableps (Atheriniformes, Anablepidae), eggs are fertilized and embryos develop to term within the ovarian follicles. Development is highly matrotrophic. During gestation, the largest term embryo of A. anableps examined had grown to a total length of 51 mm and attained a dry weight of 149 mg. The postfertilization weight increase is 298,000%. The largest term embryo of A. dowi examined had grown to a total length of 77 mm and attained a dry weight of 910 mg. The postfertilization weight increase is 843,000%. Embryonic weight increases result from nutrient transfer across the follicular placenta. This structure is formed by apposition of the maternal follicular epithelium to absorptive surface cells of the embryo's pericardial trophoderm. The latter, a ventral ramification of the pericardial somatopleure, replaces the yolk sac during early gestation. The external surface of the pericardial trophoderm develops hemispherical projections, termed vascular bulbs. Within each bulb, the vascular plexus of the trophoderm expands to form a blood sinus. Cells of the external surface of the bulbs possess microplicae. Microvilli are absent. During middle to late gestation, the juxtaembryonic follicular epithelium differentiates into two regions. One region consists of shallow, pitlike depressions within which vascular bulbs interdigitate in a “ball and socket” arrangement. Follicular pits are formed by the curvilinear distortion of the apical surfaces of follicle cells. The second region in contact with the dorsal and lateral surfaces of the embryo, is comprised of villous extensions of the hypertrophied follicular epithelium. In both regions, follicle cells appear to constitute a transporting rather than a secretory epithlium. In terms of percentage of weight increase, the follicular placenta of Anableps appears to be the most efficient adaptation for maternal-embryonic nutrient transfer in teleost fishes and closely approaches the efficiency (1.2 × 106%) of oophagy and embryonic cannibalism in lamnoid sharks.
The egg envelope (zona radiata) of the full-grown oocytes before fertilization was examined by electron microscope in eight viviparous species of Goodeidae (Cyprinodontiformes) from the Mexican plateau. The egg envelope is composed of a homogeneous electron-dense zona radiata perforated mainly by oocyte microvilli. The thickness of the zona radiata ranged from 0.5 μm (Xenoophorus captivus) to 1.5 μm (Ameca splendens). Egg envelopes of Ataeniobius toweri and Ilyodon xantusi appeared to have two layers, tentatively described as a zona radiata interna and a zona radiata externa. The most complex envelope was observed in Girardinichthys multiradiatus, which showed a small filamentous zona radiata interna and an electron-dense zona radiata externa covered by an additional flocculent layer, which is probably the gelatinous coat found in many eggs. The egg envelope of Ameca splendens, Girardinichthys viviparus, and Xenotoca eiseni displayed short external processes resembling attaching filaments, which are known from eggs of substrate-spawning teleosts. The thickness and differentiation of the zona radiata in other viviparous teleosts are compared and discussed with reference to mode of reproduction.
1. We examined the numerical dynamics in four natural populations of the least killifish [Heterandria formosaAgassiz (1855)]; to ascertain how those dynamics affected the expression of key life-history traits and, in turn, whether life-history variation among populations might be responsible for different dynamic properties. Populations were chosen from two types of communities, spring-fed rivers and lakes, to examine the relative influence of community characteristics on these relationships.
2. Populations in lakes had lower densities, more female-biased sex ratios and a smaller proportion of immature individuals than populations in rivers. Predator faunas differed between habitats and the ratio of predator to H. formosa density was higher in lakes than in rivers.
3. Females in lake populations were 35−40% larger than river females. Female size was positively correlated with the number of broods carried by a female at any given time and the number of offspring in a particular brood. These correlations and the larger body size of females in lake populations indicate that the reproductive output per female was higher in lake than river populations.
4. Female size was negatively correlated with population density in two of the four populations. After adjusting for the variation in female size, brood size and brood numbers were negatively correlated with population density in only the highest density population.
5. Average offspring size was negatively correlated with brood size in all of the populations, indicating a general trade-off between offspring size and number. The average offspring size in the highest density population was as much as 45% larger than that of all other populations, an effect independent of any phenotypic plasticity in offspring size with respect to female body size or density.
6. The effects of density on female body size are the major avenue for negative feedback of population density on the subsequent dynamics through life-history expression. Whether such an effect is stabilizing or destabilizing cannot yet be determined. If the variation in offspring size among populations is adaptive, it may be a prominent example of density-dependent life-history evolution.
Gravid ovaries were examined histologically from two species of Nomorhamphus and 21 populations of Dermogenys. In addition, changes in dry-weight throughout gestation are provided for 15 populations. The ovaries are paired organs running along the lateral body wall and are separated along most of their length. In all specimens examined, embryos are fertilized within the ovarian follicle. Viviparity in these species is divided herein into five categories designated types I–V. In types I and II the entire gestation period is intrafollicular, whereas in types III–V only the early stages of gestation are intrafollicular with the major period of development occurring in the ovarian lumen (intraluminal). Type I is characterized by the retention of a large amount of yolk throughout gestation. Superfetation is not observed. Populations of D. pusilla from Vietnam and Thailand decrease in dry-weight throughout gestation. This, coupled with the slight vascularization of the yolk sac, suggests strict lecithotrophy. Populations of D. pusilla from Singapore and Bangladesh undergo an increase in dry weight and exhibit an increased vascularization of the yolk sac, suggesting a form of unspecialized matrotrophy. Type II is characterized by a small amount of yolk, an expansion of the coelomic cavity and pericardial sac, and a simple cuboidal epithelium on the general body surfaces. Superfetation occurs with up to three broods present within a single ovary. Dermogenys pusilla from Sabah, D. orientalis and Dermogenys sp. (Sulawesi) exhibit the type II form of viviparity. Dermogenys vivipara from the eastern Philippine islands of Culion and Busuanga exhibit characteristics considered intermediate between type I and II. These results are compared with those from other viviparous species exhibiting intrafollicular gestation. In species with types III–V (intraluminal gestation), developing oocytes are restricted to a distinct ridge of ovigerous tissue extending along the entire length of the ovary. Two species, D. viviparus (Luzon, Philippines) and Dermogenys sp. (Luzon) have the type III form of viviparity. In this form, oocytes are small (0.8–1.0 mm) with little yolk reserves and embryos, covered with a simple cuboidal epithelium and possessing an expanded belly sac, are retained within the follicles until a late fin-bud stage. Type III embryos found within the ovarian lumen have a greatly expanded belly sac and remain covered by a simple cuboidal epithelium until parturition. Superfetation is present in these species with two broods observed simultaneously within a single ovary. Five species, D. megarrhamphus, D. weberi, D. viviparus (Jolo, Philippines), Nomorhamphus sp. (Sulawesi), and N. towoetii, were observed with the type IV form of viviparity. Embryos in this category are evacuated into the ovarian lumen prior to a fin-bud stage and retain a large yolk mass throughout development. Superfetation is absent in these species. A differentform of viviparity (type V) is present in D. ebrardtii in which embryos appear to obtain nutrients through a form of oophagy and aldelphophagy (feeding on developing oocytes or less-developed siblings). In all specimens with intraluminal development, atretic oocytes within the ovigerous ridge are abundant. These findings support the hypothesis that current species and generic limits may be artificial and underscores the potential of histological evidence for phylogenetic analysis of this group. J. Morphol. 234:295–317, 1997. © 1997 Wiley-Liss, Inc.
Embryonic growth and trophotaenial development are examined in two species of goodeid fish, Ameca splendens and Goodea atripinnis. During gestation of A. splendens, embryonic dry mass may increase from 0.21 mg at the onset of development to 31.70 mg at term. In G. atripinnis, embryonic dry mass ranges from 0.25 mg at the onset of development to 3.15 mg at term. Increase in mass is primarily due to the uptake of maternally derived nutrients by trophotaeniae, externalized embryonic gut derivatives. Trophotaenial development in both species is divisible into five phases. During the first phase, the anus is formed. The second phase involves dilation of the anus, enlargement of the perianal lips, differentiation of the hindgut absorptive epithelium, and formation of the trophotaenial peduncle. The third phase is characterized by a further marked hypertrophy and lateral expansion of the perianal lips that results in the formation of short trophotaenial processes. During the fourth phase, there is continued outward expansion of the inner mucosal surface of the trophotaenial peduncle that results in its eversion and lobulation. Placental function is established by this phase. Axial elongation and dichotomous branching of trophotaenial processes occurs during the fifth phase. Development of rosette and ribbon trophotaeniae differ in the degree of axial elongation during the fifth and final phase.
Embryos of the poeciliid Heterandria formosa develop to term in the ovarian follicle in which they establish a placental association with the follicle wall (follicular placenta) and undergo a 3,900% increase in embryonic dry weight. This study does not confirm the belief that the embryonic component of the follicular placenta is formed only by the surfaces of the pericardial and yolk sacs; early in development the entire embryonic surface functions in absorption. The pericardial sac expands to form a hood-like structure that covers the head of the embryo and together with the yolk sac is extensively vascularized by a portal plexus derived from the vitelline circulation. The hood-like pericardial sac is considered to be a pericardial amnion-serosa. Scanning and transmission electron microscopy reveal that during the early and middle phases of development (Tavolga's stages 10–18 for Xiphophorus maculatus) the entire embryo is covered by a bilaminar epithelium whose apical surface is characterized by numerous, elongate microvilli and coated pits and vesicles. Electron-lucent vesicles in the apical cytoplasm appear to be endosomes while a heterogeneous group of dense-staining vesicles display many features characteristic of lysosomes. As in the larvae of other teleosts, cells resembling chloride cells are also present in the surface epithelium. Endothelial cells of the portal plexus lie directly beneath the surface epithelium of the pericardial and yolk sacs and possess numerous transcytotic vesicles. The microvillous surface epithelium becomes restricted to the pericardial and yolk sacs late in development when elsewhere on the embryo the non-absorptive epidermis differentiates. We postulate that before the definitive epidermis differentiates, the entire embryonic surface constitutes the embryonic component of the follicular placenta. The absorptive surface epithelium appears to be the principle embryonic adaptation for maternal-embryonic nutrient uptake in H. formosa, suggesting that a change in the normal differentiation of the surface epithelium was of primary importance to the acquisition of matrotrophy in this species. In other species of viviparous poeciliid fishes in which there is little or no transfer of maternal nutrients, the embryonic surface epithelium is of the non-absorptive type.
1.1. The osmolarity of the follicular fluid and of the maternal plasma was determined and analyses of glucose, total sugars, total proteins, total lipids and amino acids carried out.2.2. It was found that the mean osmolarity of the follicular fluid was 52.48 mOsm/kg higher than the osmolarity of the plasma (324.2 ± 20.6 mOsm/kg) so that the embryos were always immersed in a liquid medium owing to the osmotic influx of water into the follicle.3.3. It was shown that the embryotrophe was rich in lipids (76.2 ± 14.0 mg/100 ml) and amino acids, with the amino acid concentration exceeding normal values for human plasma.
Embryos of the viviparous poeciliid fish, Heterandria formosa, develop to term in the ovarian follicle where they undergo a 3,900% increase in embryonic dry weight. Maternal-embryonic nutrient transfer occurs across a follicular placenta that is formed by close apposition of the embryonic surface (i.e., the entire body surface during early gestation and the pericardial amnionserosa during mid-late gestation) to the follicular epithelium. To complement our recent study of the embryonic component of the follicular placenta, we now describe the development and fine structure of the maternal component of the follicular placenta. Transmission electron microscopy reveals that the ultrastructure of the egg envelope and the follicular epithelium that invests vitellogenic oocytes is typical of that described for teleosts. The egg envelope is a dense matrix, penetrated by microvilli of the oocyte. The follicular epithelium consists of a single layer of cuboidal cells that lack apical microvilli, basal surface specializations, and junctional complexes. Follicle cells investing the youngest embryonic stage examined (Tavolga's and Rugh's stage 5–7 for Xiphophorus maculatus) also lack apical microvilli and basal specializations, but possess junctional complexes. In contrast, follicle cells that invest embryos at stage 10 and later display ultrastructural features characteristic of transporting epithelial cells. Apical microvilli and surface invaginations are present. The basal surface is extensively folded. Apical and basal coated pits are present. The cytoplasm contains a rough endoplasmic reticulum, Golgi complexes, and dense staining vesicles that appear to be lysosomes. The presence of numerous apically located electron-lucent vesicles that appear to be derived from the apical surface further suggests that these follicle cells may absorb and process follicular fluid. The egg envelope, which remains intact throughout gestation and lacks perforations, becomes progressively thinner and less dense as gestation proceeds. We postulate that these ultrastructural features, which are not present in the follicles of the lecithotrophic poeciliid, Poecilia reticulata, are specializations for maternal-embryonic nutrient transfer and that the egg envelope, follicular epithelium, and underlying capillary network form the maternal component of the follicular placenta. © 1994 Wiley-Liss, Inc.
Reproductive events tend to be synchronized in natural populations ofXiphophorus variatus. Males physically resembling one another tend to mature at the same rate and time. This coordinate development has also been seen in the laboratory. We hypothesize that juveniles resembling each other experience fewer aggressive responses from males than do juveniles without ‘look-alikes’, because of habituation of aggression. This would decrease social inhibition and permit their synchronous development.
Females have an ovarian cycle. In the laboratory, crowding stress causes a suspension of breeding while a return to uncrowded conditions permits its resumption. Females released simultaneously from crowding tend to be synchronized in subsequent broods, although the synchrony deteriorates with time. Synchronizing events are shown to occur in natural populations.
The consequences of reproductive synchrony in males and females are briefly discussed.
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