ArticlePDF Available

Protogynous Sex Change in the Reed Frog Hyperolius viridiflavus

Authors:

Abstract and Figures

Observations on captive reed frogs Hyperolius viridijlavus ommatostictus showed that seven out of 24 females changed into males. Sex change occurred without any hormone treatment and resulted in completely functional males. The adaptive value is discussed in terms of maximizing life-time reproductive success. Hyperolius r. ommatostictus is the first amphibian known to show functional sex reversal.
Content may be subject to copyright.
A preview of the PDF is not available
... Protogynous sex change, in which adult (e.g., sexually mature) females transform into reproductively active males, has only been documented in 2 anuran species. Both are hyperoliids, and both belong to the Hyperolius viridiflavus species complex (Grafe and Linsenmair 1989;Wieczorek et al. 2000). Protogynous sex change might maximize lifetime reproductive success in highly seasonal environments where mortality may be sex-dependent (Grafe and Linsenmair 1989). ...
... Both are hyperoliids, and both belong to the Hyperolius viridiflavus species complex (Grafe and Linsenmair 1989;Wieczorek et al. 2000). Protogynous sex change might maximize lifetime reproductive success in highly seasonal environments where mortality may be sex-dependent (Grafe and Linsenmair 1989). In these species, a breeding population can consist of primary males, females, and secondary males (e.g., females that have transformed into males). ...
... In these species, a breeding population can consist of primary males, females, and secondary males (e.g., females that have transformed into males). There are no significant differences in the body sizes of primary males and females, and as a result the secondary males are also comparable in size to primary males (Grafe and Linsenmair 1989). This finding suggests that protogynous sex change may be correlated with a reduction in SSD (e.g., a shift to SSM). ...
Article
Full-text available
Sexual size dimorphism (SSD) is shaped by multiple selective forces that drive the evolution of sex-specific body size, resulting in male or female-biased SSD. Stronger selection on one sex can result in an allometric body-size scaling relationship consistent with Rensch's rule or its converse. Anurans (frogs and toads) generally display female-biased SSD, but there is variation across clades and the mechanisms driving the evolution of SSD remain poorly understood. We investigated these topics in a diverse family of African treefrogs (Hyperoliidae). Hyperoliids display traits considered rare among amphibians, including sexual dichromatism and protogynous sex change. Using phylogenetic comparative methods, we tested if adult ecology, sexual dichromatism, and sex change were predictors of body size or SSD. We also tested whether hyperoliids displayed allometric interspecific body-size-scaling relationships. We found a majority of hyperoliid taxa display female-biased SSD, but that adult ecology and sexual dichromatism are poor predictors of sex-specific body size and SSD. Regardless of the groupings analyzed (partitioned by clades or traits), we found support for isometric body-size scaling. However, we found that sex change is a significant predictor of SSD variation. Species in the Hyperolius viridiflavus complex, which putatively display this trait, show a significant reduction in SSD and are frequently sexually monomorphic in size. Although protogynous sex change needs to be validated for several of these species, we tentatively propose this trait is a novel mechanism influencing anuran body size evolution. Beyond this association, additional factors that shape the evolution of anuran body size and SSD remain elusive.
... Much work would be necessary to determine the existence and relevance, or true absence, of natural functional hermaphrodism in frogs. However, Grafe and Linsenmair's (1989) H. viridiflavus came from Tanzania, where changing one's legal name and gender is impossible and consensual same-sex sexuality is punishable by life in prison (Chiam et al. 2017;Ramon Mendos 2019). ...
... This both motivates my study of hatching and generates testable hypotheses.Herpetology still harbors unexplored mysteries, including isolated studies reporting unexplained phenomena that may serve as motivating possibilities. Natural sex change in frogs is one such case.In a laboratory study of individually identifiable Hyperolius viridiflavus, 7 of 24 females became males(Grafe & Linsenmair 1989). These individuals laid viable eggs, then developed vocal sacs, called, fought with primary males, amplexed females, and fertilized eggs.reproductive ...
Chapter
Full-text available
How biologists and other humans understand life has been shaped by our social history and mammalian biology, which inform the questions we ask. Compared with other tetrapods, amphibians and reptiles show amazing diversity in reproductive biology and life history. Herpetology reveals this variation, expanding what we know as possible and enabling us to ask new questions. Queer perspectives, informed by the lives of diverse biologists, influence what we notice, ask, and investigate. Combining human and herpetological diversity, and attending to queer observations, offers great potential for transformative discoveries.
... In some cases, one of the types of gonads may not be fully functional [e.g., gobies (Cole and Hoese 2001) or spirochid trematodes (Anderson and Cribb 1994;Platt and Blair 1996)]. In bufonid toads, the testes of mature males are capped by Bidder's organ, which contains maturing oocytes (Farias et al. 2002), but there are apparently no reports of self-fertilization or functional hermaphroditism [personal communication, Marvalee H. Wake; but see Grafe and Linsenmair (1989)]. However, both sex change (see below) and hermaphroditism are easily induced experimentally (review in Wallace et al. 1999), so there would seem to be potential for selection to produce either sequential or simultaneous hermaphroditism. ...
... 11) discuss the role of estrogen signaling pathways in sex change in teleosts. Although amphibians have chromosomal sex determination, as far as is known (Wallace et al. 1999), there is one report of protogynous sequential hermaphroditism in a laboratory population of a frog (Grafe and Linsenmair 1989). In angiosperms, sequential hermaphroditism is rarer, but it has evolved many times (Freeman et al. 1980;Charnov 1982) and involves very similar phenomena (Vega-Frutis et al. 2014). ...
Chapter
Full-text available
A sexual system is the pattern of gender allocation that characterizes a species. In both plants and animals, simultaneous hermaphroditism and dioecy are the most common and stable sexual systems. Other sexual systems, sequential hermaphroditism, environmental sex determination, gynodioecy, androdioecy, and trioecy, are less stable and less widely distributed. The boundaries between these sexual systems are not always clear, largely because phenotypic plasticity is an important and prevalent component of sexual reproduction. One can view sexual systems in the Metazoa as lying on a gradient of phenotypic plasticity from simultaneous hermaphroditism at the high end through sequential hermaphroditism and environmental sex determination to genetically determined dioecy, which has a minimum of phenotypic plasticity in sex allocation. The distribution of sexual systems across the Metazoa gave rise to Williams’ Paradox, which states that the pattern is best explained by phylogeny rather than sex allocation theory. Today, sex allocation theory seems to explain transitions in sexual system in those taxa with labile sexual systems adequately. However, the stability of either dioecy or simultaneous hermaphroditism in many major taxa, such as phyla and classes, remains inexplicable. While in angiosperms the evolutionary pathways between dioecy and simultaneous hermaphroditism are fairly well understood, a plausible evolutionary sequence for transitions between dioecy and simultaneous hermaphroditism in animals has been lacking. Here, the proposal is made that it is useful to view transitions from simultaneous hermaphroditism to dioecy as the result of selection for decreasing phenotypic plasticity and vice versa. A scenario for evolutionary transitions between simultaneous hermaphroditism and dioecy, in animals, through intermediate stages of sequential hermaphroditism and environmental sex determination is proposed.
... Sexually mature males frequently maintain juvenile coloration throughout adulthood. Phase F, the adult phase, maybe a highly variable color pattern with distinct morphs (Grafe & Linsenmair, 1989;Schiøtz, 1999). The present study demonstrated that the coloration of adult H. pickersgilli females is relatively uniform. ...
Article
Full-text available
Globally, the threats of habitat loss and disease on amphibian survival have necessitated the creation of ex-situ insurance populations as a conservation tool. We initiated a captive breeding project to create an insurance population for the endangered Pickersgill's reed frog (Hyperolius pickersgilli Raw, 1982) at the Johannesburg Zoo from parents collected from KwaZulu-Natal Province, South Africa, in 2017. We found that this species has seven developmental life stages, each with unique management requirements. The quiescent tadpoles hatched 6-8 days after the eggs were laid and remained at this stage for 2 days. The next stage, the developing tadpoles, showed no form of cannibalism or carrion feeding. The external appearance of the first leg (the right hind) occurred 5-6 weeks after the tadpoles hatched, and the metamorph stage was reached after 7-8 weeks. The metamorph stage lasted 3-5 days, after which tail resorption was complete and the froglet stage reached. Froglets could not be sexed externally, although body color changed based on the amount of light present at the resting place. Sub-adults were 6 months and older with adult coloration and sex differentiation visible even with color change. Adults were older than 18 months and fully developed and sexually mature, displaying amplexus, oviposition, and external fertilization. A greater understanding of Pickersgill's reed frog's developmental stages and physiological and environmental needs can improve captive breeding and subsequent release of the frogs, facilitate captive breeding elsewhere, and improve the species' conservation status.
... Species selection will be critical for comparative studies of sex dif- (Avise & Mank, 2009). Several species of African reed frogs (Grafe & Linsenmair, 1989) would be of great interest, as they could reveal if and how aging trajectories change with a sex change. Ideally, in each case, we would identify two or more species or populations of interest from more than one major branch of the animal tree of life to ensure that what we observe is a general phenomenon rather than a species-specific oddity. ...
Article
Full-text available
Sex differences in aging occur in many animal species, and they include sex differences in lifespan, in the onset and progression of age‐associated decline, and in physiological and molecular markers of aging. Sex differences in aging vary greatly across the animal kingdom. For example, there are species with longer‐lived females, species where males live longer, and species lacking sex differences in lifespan. The underlying causes of sex differences in aging remain mostly unknown. Currently, we do not understand the molecular drivers of sex differences in aging, or whether they are related to the accepted hallmarks or pillars of aging or linked to other well‐characterized processes. In particular, understanding the role of sex‐determination mechanisms and sex differences in aging is relatively understudied. Here, we take a comparative, interdisciplinary approach to explore various hypotheses about how sex differences in aging arise. We discuss genomic, morphological, and environmental differences between the sexes and how these relate to sex differences in aging. Finally, we present some suggestions for future research in this area and provide recommendations for promising experimental designs. Sex difference in aging occurs across the animal kingdom, but there is considerable variation and they are not universal. The processes leading to sex‐specific aging are poorly understood and might originate in sex‐specific genome architecture, organismal biology, or environmental interactions. Here, we take a comparative approach to review the various hypotheses and suggest promising areas of research for further study.
... Occasional reports on natural sex change in adult anurans (e.g. [147] in Hyperolius viridiflavus) require further examination. ...
Article
Full-text available
Triggers and biological processes controlling male or female gonadal differentiation vary in vertebrates, with sex determination (SD) governed by environmental factors or simple to complex genetic mechanisms that evolved repeatedly and independently in various groups. Here, we review sex evolution across major clades of vertebrates with information on SD, sexual development and reproductive modes. We offer an up-to- date review of divergence times, species diversity, genomic resources, genome size, occurrence and nature of polyploids, SD systems, sex chromosomes, SD genes, dosage compensation and sex-biased gene expression. Advances in sequencing technologies now enable us to study the evolution of SD at broader evolutionary scales, and we now hope to pursue a sexomics integrative research initiative across vertebrates. The vertebrate sexome comprises interdisciplinary and integrated information on sexual differentiation, development and reproduction at all biological levels, from genomes, transcriptomes and proteomes, to the organs involved in sexual and sex-specific processes, including gonads, secondary sex organs and those with transcriptional sex-bias. The sexome also includes ontogenetic and behavioural aspects of sexual differentiation, including malfunction and impairment of SD, sexual differentiation and fertility. Starting from data generated by high-through- put approaches, we encourage others to contribute expertise to building understanding of the sexomes of many key vertebrate species. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.
... Therefore, it is possible that the hermaphroditism we documented may be related to chemical exposure from agricultural practices (Hayes et al. 2002). Protogynous hermaphroditism (sex change from female to male) is also a possibility, although typically restricted to cases where it maximises an individual's lifetime reproductive success (Grafe and Linsenmair 1989). ...
Article
Anurans can display a host of intriguing sexual syndromes, including hermaphroditism and sex reversal. Using a multifaceted approach for diagnosing and characterising hermaphroditism in the endangered anuran species Rana mucosa, we tracked changes in female reproductive status using hormone monitoring, ultrasound examinations, individual life history, fertilisation records and post-mortem findings. Seven individuals originally sexed as females developed secondary male sexual characteristics, behaviour and hormone profiles and, in some cases, had testicular tissue despite having previously laid eggs. Our results suggest that reproductive technologies can shed light on life history patterns and reproductive anomalies that may affect endangered anuran survival.
... A hermaphrodite is an individual, plant or animal, that produces both eggs and sperm over the course of its lifetime and is capable of reproducing in both sexual roles. In animals, hermaphroditism is found in many (but not all) invertebrate classes and phyla but among vertebrates occurs only in the teleosts (although there is one report of sequential hermaphroditism in a laboratory population of frogs (Grafe and Linsenmair, 1989)). There are cases in which a male or a female may, anomalously, produce either eggs or sperm, or organs associated with the opposite sex, which are not functional. ...
Chapter
Full-text available
... This method was chosen to ensure that total fecundity for the individual was recorded instead of collecting egg deposits in the water which might represent a fraction of the eggs laid by a female in a single night. In order to add these data to a larger test of a correlation between egg counts and female body size (Snout-Urostyle-Length (SUL)) to examine a potential size-fecundity relationship, we combined all available data on total egg clutches, egg diameters, and characteristics for other species of Afrixalus and Hyperolius (Grafe and Linsenmair, 1989;Schiøtz, 1999;Rödel, 2000;Channing, 2001;Channing and Howell, 2006;Pickersgill, 2007;Kouamé et al., 2015). As many of these values are listed as ranges, we used the largest recorded number of eggs and largest body size. ...
... Sex reversal has been observed in several species in the laboratory. In captivity, some protogyneous individuals of Hyperolius viridiflavus with reduced fertilization rates were observed under low-male density conditions (75), and some protandreous individuals of Triturus alpestris were found under conditions of food deprivation (76). A wellknown example of artificial sex change is found in Bufo bufo, in which chirurgical removal of the testes of sexually mature males is followed by the development of the Bidder's organ into functional ovaries (77). ...
Article
Full-text available
In vertebrates, sex organs are generally specialized to perform a male or female reproductive role. Acquisition of the Müllerian duct, which gives rise to the oviduct, together with emergence of the Amh/Amhr2 system favored evolution of viviparity in jawed vertebrates. Species with high sexspecific reproductive adaptations have less potential to sex reverse, making intersex a nonfunctional condition. Teleosts, the only vertebrate group in which hermaphroditism evolved as a natural reproductive strategy, lost the Müllerian duct during evolution. They developed for gamete release complete independence from the urinary system, creating optimal anatomic and developmental preconditions for physiological sex change. The common and probably ancestral role of Amh is related to survival and proliferation of germ cells in early and adult gonads of both sexes rather than induction of Müllerian duct regression. The relationship between germ cell maintenance and sex differentiation is most evident in species in which Amh became the master male sex–determining gene. Expected final online publication date for the Annual Review of Animal Biosciences Volume 7 is February 15, 2019. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Article
Full-text available
In two-choice discrimination experiments, females of Hyperolius marmoratus preferred the calls of lower frequency of the pair of stimuli. This preference was not shown in mating patterns observed in natural choruses, but is when females are phonotactically orienting in small choruses in an experimental enclosure. With an increase in chorus size, the mating pattern shifts from size-based, non-random (with some evidence of size-assortative) mating to random mating. This is the first time that frequency-based mate-choice by female anurans has been associated with chorus size, and hence with the sonic complexity of the acoustic environment.
Article
Full-text available
Evidence is presented that individuals of a large number of dioecious and subdioecious plant species are able to alter their sexual state in response to changes in the ambient environment and/or changes in size or age. We suggest that lability of sexual expression probably has survival value where a significant portion of the females must otherwise bear the cost of fruit production in unfavorable environments. We demonstrate that in patchy environments of the proper scale and variability in quality, labile sexual expression will enhance an individual's genetic contribution to the next generation.
Article
Samples of alligators from wild and "farm" populations exhibited disproportionate sex ratios. Males predominated among young alligators from wild populations, whereas females were much more abundant than males in the farm population, where resources were superabundant. These results and other considerations lead us to hypothesize that environmental factors influence sex determination in alligators. During favorable environmental conditions natural selection is expected to favor a preponderance of the sex whose individuals exhibit the greater environmentally associated variation in relative fitness. We hypothesize that environmentally associated variation in age at sexual maturity of females produces sufficient variation in relative fitness of females to result in selection for low sex ratios during periods of resource abundance.
Article
When the life history functions B (E) and P (E)-fecundity and postbreeding survival-are subject to environmentally induced fluctuations, one of two patterns is selected for: If the functions are concave (iteroparity in constant environments), the optimal population is monomorphic. Variation in B (E) selects for reduced effort in all individuals; variation in P (E) for increased breeding. If functions are convex (semelparity in constant environments) and fecundity is the parameter at issue, the optimal population can be polymorphic, with only a fraction of the population reproducing annually. Increasing the severity of fluctuations reduces the optimal value of this proportion, even if the average rate of reproductive success is not changed.
Article
Thesis (Ph. D.), 1981. Typescript (photocopy). Includes vita. Includes bibliographical references (leaves 236-250).