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Categories of oviposition and tadpole development sites (identified as primarily aquatic or terrestrial), types of amplexus, and parental care for taxa included in this
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Frog reproductive modes are complex phenotypes that include egg/clutch characteristics, oviposition site, larval development, and sometimes, parental care. Two evident patterns in the evolution of these traits are the higher diversity of reproductive modes in the tropics and the apparent progression from aquatic to terrestrial reproduction, often a...
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... gathered data from the literature on various aspects of reproduction in hylid and leptodactylid species. We divided reproductive mode into components based on life stage and whether they were associated primarily with aquatic or ter- restrial sites (table 1). Specifically, we focused on oviposi- tion site, tadpole development site, whether species have ex- posed or hidden amplexus, the presence or absence of parental care, and species biogeographic distribution (table 1; fig. ...Similar publications
Evolutionary radiations on continents are less well understood and appreciated than those occurring on islands. The extent of ecological influence on species divergence can be evaluated to determine whether a radiation was ultimately the outcome of divergent natural selection or else arose mainly by non-ecological divergence. Here, we used phylogen...
The evolution of exclusive paternal care in arthropods is influenced by both natural and sexual selection. Male care may simultaneously increase egg protection against natural enemies and male attractiveness to ovipositing females. When caring males desert or die, their clutches may be adopted either by females that provide flexible compensation of...
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... Previous comparative studies of anurans have shown that high levels of sperm competition are also likely to be the main factor selecting for larger testes or ejaculates, while males of species with hidden nests (i.e. eggs not exposed to sneakers) and a low sperm competition risk have relatively smaller testes [6,15,67,68]. In this context, our results suggest that paternal care may lower the sperm competition risk via clutch guarding. ...
... Thus, by protecting their clutches from potential sneakers, glassfrog males may reduce the need to invest in sperm production, ultimately decreasing testes size or limiting its evolutionary increase. Similarly, gladiator frogs in the Boana faber group that aggressively defend constructed nests against intruder males, and exhibit short-term paternal care, also have smaller testes compared to closely related species [67]. Although few studies have assessed paternity in glassfrogs, to date there is no evidence of sperm competition or multiple paternity in species that provide paternal care (Hyalinobatrachium valerioi [71], H. cappellei [72]). ...
... Besides clutch size, the type of clutch ( jelly masses or foam nests), mating system and spawning location (e.g. aquatic versus terrestrial, hidden versus exposed) are other factors that have previously been reported to influence ejaculate expenditure, and thus testes size in anurans [15,67,68,94]. It seems likely that variation in egg-clutch structure (e.g. ...
In males, large testes size signifies high sperm production and is commonly linked to heightened sperm competition levels. It may also evolve as a response to an elevated risk of sperm depletion due to multiple mating or large clutch sizes. Conversely, weapons, mate or clutch guarding may allow individuals to monopolize mating events and preclude sperm competition, thereby reducing the selection of large testes. Herein, we examined how paternal care, sexual size dimorphism (SSD), weaponry and female fecundity are linked to testes size in glassfrogs. We found that paternal care was associated with a reduction in relative testes size, suggesting an evolutionary trade-off between testes size and parenting. Although females were slightly larger than males and species with paternal care tended to have larger clutches, there was no significant relationship between SSD, clutch size and relative testes size. These findings suggest that the evolution of testes size in glassfrogs is influenced by sperm competition risk, rather than sperm depletion risk. We infer that clutch guarding precludes the risk of fertilization by other males and consequently diminishes selective pressure for larger testes. Our study highlights the prominent role of paternal care in the evolution of testes size in species with external fertilization.
... The most discussed of these hypotheses proposes direct development as an alternative trait resulting from evolutionary processes linked to the action of biotic factors, such as predation of aquatic eggs and larvae and/or competition for reproductive sites [3,11,12]. Also, the hidden amplexus of certain terrestrial breeders (some species of the families Hylidae and Leptodactylidae) may exemplify how sexual selection (competition among males for reproductive females and polyandry avoidance) molded the evolution of reproductive modes in anurans [13]. Alternatively, the abiotic environment has also been presented as a potential selective force in the evolution of direct development. ...
Different environmental and biological factors can originate and support different alternative life histories in different taxonomic groups. Likewise, these factors are important for the processes that assemble and structure communities. Amphibians, besides being highly susceptible to environmental conditions, have various reproductive strategies, such as the direct development of individuals. Several hypotheses have been raised about possible selective pressures related to the emergence of direct development in anurans, as well as the relationship between environmental characteristics and the occurrence of these species. Such investigations, however, have mainly focused on specific clades and/or regions. Here, we use structural equation modelling to investigate the relationships between different abiotic (temperature, precipitation, humidity, and terrain slope) and biotic (phylogenetic composition and functional diversity) factors and the proportion of species with direct development in 766 anuran communities of the Atlantic Forest, a biome with a vast diversity of anuran species and high environmental complexity. Anuran communities with higher proportions of direct developing species were found to be mainly influenced by low potential evapotranspiration, low temperature seasonality, and high functional diversity. Phylogenetic composition and terrain slope were also found to be important in determining the occurrence of these species in Atlantic Forest communities. These results show the importance of these factors in the structuring of these communities and provide important contributions to the knowledge of direct development in anurans.
... Other species lay their eggs inside cavities, burrows, or small water-filled crevices in terrestrial plants, for example, Hylophorbus rufescens lays eggs in damp cavities close to the ground level (Menzies 1976); Oreophryne species use hollow aerial tubers of epiphytes (Matsui et al. 2013); and Eleutherodactylus species use cavities in tree ferns (Estrada & Hedges 1996). Parental care, in the form of egg attendance, has been associated with terrestrial oviposition of anuran species on wet substrates as a behaviour exhibited by the parent to improve the chances of survival for its offspring (Duellman & Trueb 1986), although this correlation of parental attendance and terrestrial reproduction varies between different taxonomic groups (Zamudio et al. 2016). ...
... A general shift toward reproduction in terrestrial habitats has likely evolved as a response to intense predation on aquatic eggs and larvae (Alford 1999, Magnusson & Hero 1991, although predation also constitutes a major threat in non-aquatic environments (Warkentin 1995, Warkentin et al. 2005). In addition, intense intra-sexual selection likely has favored terrestrial reproduction due to a reduction in simultaneous polyandry and the associated risks of sperm competition in non-aquatic environments (Zamudio et al. 2016). ...
... Especially in tropical environments, which are not only hotspots of biodiversity in terms of species numbers but also with respect to reproductive strategies (Hödl 1990), we see the full spectrum from aquatic to terrestrial reproduction. Given that terrestrial environments are hostile for anamniotic eggs due to the high risks of desiccation (Touchon & Worley 2015), physical damage, predation, and exposure to diseases (Martin & Carter 2013), evolutionary transitions toward terrestrial reproduction required considerable behavioral, physiological, and morphological adaptations (Zamudio et al. 2016). Nonetheless, the benefits of invading non-aquatic habitats to occupy novel ecological niches likely exceeded the costs of adapting to terrestrial reproduction, and parenting often played a key role in facilitating this transition ( Figure 1). ...
Parenting is considered a key evolutionary innovation that contributed to the diversification and expansion of vertebrates. However, we know little about how such diversity evolved. Amphibians are an ideal group in which to identify the ecological factors that have facilitated or constrained the evolution of different forms of parental care. Among, but also within, the three amphibian orders—Anura, Caudata, and Gymnophiona—there is a high level of variation in habitat use, fertilization mode, mating systems, and parental sex roles. Recent work using broad phylogenetic, experimental, and physiological approaches has helped to uncover the factors that have selected for the evolution of care and transitions between different forms of parenting. Here, we highlight the exceptional diversity of amphibian parental care, emphasize the unique opportunities this group offers for addressing key questions about the evolution of parenting, and give insights into promising novel directions of research.
Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics, Volume 54 is November 2023. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
... eggs and tadpoles) from aquatic predators, and allows species to exploit a greater diversity of habitats. Additionally, terrestrial reproduction may be favoured by sexual selection because it moves breeding pairs away from large congregations of conspecifics, thereby reducing competition for mates at immediate timescales and decreasing polyandry at evolutionary timescales [18]. Yet while adults of many species are largely terrestrial, larvae (tadpoles) generally remain aquatic. ...
... In general, a role for nest choice in sexual selection is assumed in other species-including those that perform courtship marches and some burrow builders-but detailed studies are lacking, and observations are largely anecdotal. Counter to the lore that terrestrial reproduction in anuran species is driven by natural selection related to predation, Zamudio and colleagues [18] demonstrated that intrasexual selection is a major driver of diversity in anuran reproductive strategies. Linking evolutionary patterns to individual-and species-level behavioural variation is a challenge for future research. ...
Amphibians exhibit an incredible diversity of reproductive and life-history strategies, including various forms of nest construction and nesting behaviour. Although anuran amphibians (frogs and toads) are not known for their nests, nesting behaviour in this clade—broadly defined as a location chosen or constructed for eggs and young—is tightly linked to the amphibious lifestyle of this group. Transitions to increasingly terrestrial living have driven reproductive diversity in anurans, including the repeated, independent evolution of nests and nesting. Indeed, a core feature of many notable anuran adaptations—including nesting behaviour—is the maintenance of an aquatic environment for developing offspring. The tight link between increasingly terrestrial reproduction and morphological, physiological and behavioural diversity in anurans provides inroads for studying the evolutionary ecology of nests, their architects and their contents. This review provides an overview of nests and nesting behaviour in anurans, highlighting areas where additional work may be particularly fruitful. I take an intentionally broad view of what constitutes nesting to highlight what we can learn from thinking and researching comparatively across anurans and vertebrates more broadly.
This article is part of the theme issue ‘The evolutionary ecology of nests: a cross-taxon approach’.
... Trophic egg provisioning is common in species that reproduce in phytotelmata (e.g., bromeliads, tree holes), such as frogs in the families Dendrobatidae (e.g., Pröhl and Hödl, 1999) and Rhacophoridae (e.g., Kam et al., 1996), probably related to limited food resources in these microhabitats (Wells, 2007;Brown et al., 2008). However, tadpoles developing in phytotelmata may benefit from reduced aquatic predation and competition (Magnusson and Hero, 1991;Brown et al., 2008;Zamudio et al., 2016). In leptodactylids, foam nests protect offspring from aquatic predators and desiccation (Downie, 1988(Downie, , 1990 and divergence time estimates suggest that this trait evolved in the warm climates of the Eocene, followed by rapid diversification during a cold and dry period at the Oligocene/Miocene transition (Fouquet et al., 2013). ...
... Parental care behaviours observed in species of the genus Leptodactylus. A) Leptodactylus latrans female attending the eggs in the foam nest (adapted fromZamudio et al., 2016). B) Aggressive behaviour of an attending female of L. latrans (adapted from ...
Amphibians exhibit diverse parental care behaviours, which may be performed by the female, male or both parents. In the Neotropical family Leptodactylidae, frogs in the genus Leptodactylus exhibit different parenting behaviours. The repertoire of care behaviours includes egg/nest attendance, nest chamber sealing, tadpole feeding with trophic eggs, and tadpole attendance associated with complex behaviours, such as pumping behaviour and channel digging. Based on the available information, we found that 23.8% of Leptodactylus species are known to exhibit post-fertilization parental care. Future studies should focus on mechanisms involved in parent-offspring communication, including acoustic and chemical signals. Moreover, behaviours such as provisioning with trophic eggs are not well understood and deserves further investigation. Because of these complex parental care behaviours, tadpole schooling, and relative easy observation, frogs in the genus Leptodactylus represent excellent models for studies interested in parent-offspring communication and evolution of parental care.
... We suggest that one of the biggest challenges for similar studies in amphibians is to understand the processes underlying these patterns of reproductive-mode evolution [85][86][87][88] . The most general pattern is the frequent origins of non-aquatic reproduction, including the many species with direct development in all three groups. ...
Amphibians have undergone important evolutionary transitions in reproductive modes and life-cycles. We compare large-scale macroevolutionary patterns in these transitions across the three major amphibian clades: frogs, salamanders, and caecilians. We analyse matching reproductive and phylogenetic data for 4025 species. We find that having aquatic larvae is ancestral for all three groups and is retained by many extant species (33–44%). The most frequent transitions in each group are to relatively uncommon states: live-bearing in caecilians, paedomorphosis in salamanders, and semi-terrestriality in frogs. All three groups show transitions to more terrestrial reproductive modes, but only in caecilians have these evolved sequentially from most-to-least aquatic. Diversification rates are largely independent of reproductive modes. However, in salamanders direct development accelerates diversification whereas paedomorphosis decreases it. Overall, we find a widespread retention of ancestral modes, decoupling of trait transition rates from patterns of species richness, and the general independence of reproductive modes and diversification. Here, the authors use reproductive mode data with matching phylogenetic data to explore the evolution of reproductive mode, transitions between reproductive modes, and diversification rates in amphibians.
... Amphibians show a remarkable variety of mating strategies and parental sex roles compared to mammals and birds, including widespread polyandry and male uniparental care (Duellman, 1989;Schulte et al., 2020;Wells, 1977;Zamudio et al., 2016). Such behavioral diversity provides natural comparison groups to test alternative hypotheses about sex differences in spatial abilities. ...
Sex differences in vertebrate spatial abilities are typically interpreted under the adaptive specialization hypothesis, which posits that male reproductive success is linked to larger home ranges and better navigational skills. The androgen spillover hypothesis counters that enhanced male spatial performance may be a byproduct of higher androgen levels. Animal groups that include species where females are expected to outperform males based on life-history traits are key for disentangling these hypotheses. We investigated the association between sex differences in reproductive strategies, spatial behavior, and androgen levels in three species of poison frogs. We tracked individuals in natural environments to show that contrasting parental sex roles shape sex differences in space use, where the sex performing parental duties shows wider-ranging movements. We then translocated frogs from their home areas to test their navigational performance and found that the caring sex outperformed the non-caring sex only in one out of three species. In addition, males across species displayed more explorative behavior than females and androgen levels correlated with explorative behavior and homing accuracy. Overall, we reveal that poison frog reproductive strategies shape movement patterns but not necessarily navigational performance. Together this work suggests that prevailing adaptive hypotheses provide an incomplete explanation of sex differences in spatial abilities.
... 2.3 km grid size), and the dataset we used may only give a crude estimate of the climatic conditions relevant for each species. In addition, it is also possible that the social environment, i.e., mating opportunities, have also shaped the evolution of male and female parental care, as has been found in other early vertebrate groups 9,12,[79][80][81] . Unfortunately, information on genetic and social mating systems, or other details of life history such as longevity or pace-of-life are largely missing for most salamander species. ...
Complex parenting has been proposed to contribute to the evolutionary success of vertebrates. However, the evolutionary routes to complex parenting and the role of parenting in vertebrate diversity are still contentious. Although basal vertebrates provide clues to complex reproduction, these are often understudied. Using 181 species that represent all major lineages of an early vertebrate group, the salamanders and newts (Caudata, salamanders henceforth) here we show that fertilisation mode is tied to parental care: male-only care occurs in external fertilisers, whereas female-only care exclusively occurs in internal fertilisers. Importantly, internal fertilisation opens the way to terrestrial reproduction, because fertilised females are able to deposit their eggs on land, and with maternal care provision, the eggs could potentially develop outside the aquatic environment. Taken together, our results of a semi-aquatic early vertebrate group propose that the diversity and follow-up radiation of terrestrial vertebrates are inherently associated with a complex social behaviour, parenting.
... Egg and larvae predation in aquatic environments has been suggested as the main evolutive force driving the terrestriality and the diversification of reproductive modes in frogs (Haddad & Prado 2005), especially in the Tropics (Gomez-Mestre et al. 2012). However, the putative fitness loss caused by polyandry (which is favored by external fertilization) likely can also act as a selective factor for the diversification of reproductive modes (Zamudio et al. 2016). Although most anurans present direct deposition of eggs in standing water where exotrophic tadpoles develop (the most basal reproductive mode) (Wells 2007), almost 40 different reproductive modes were reported for the group (Haddad & Prado 2005;Pombal & Haddad 2007). ...
... Anurans present complex mating systems, displays, and acoustic signals related to mate selection and mating opportunities (Sullivan & Kwiatkowski 2007). Sexual selection is a strong selective force driving the evolution of social behavior, affecting several aspects of reproduction in vertebrates, such as parental care, sexual dimorphism, territoriality, reproductive mode, and sexual maturation (Howard 1980;Agrawal 2001;Andersson & Simmons 2006;Zamudio et al. 2016). ...
Reproductive strategies are one of the more fascinating aspects of Anuran biology and are likely affected by species habitat use and availability of reproductive sites. The Cerrado endemic Pithecopus oreades is a habitat specialist that reproduces in seasonal high-altitude rocky streams in Central Brazil. Herein, we describe its reproductive behavior based on observations made during two consecutive reproductive seasons in a high-altitude stream located in an open field area in Central Brazil. The reproductive activity of P. oreades occurs during the rainy season, from the very first rains, and lasts about 3 months. The species is nocturnal, showing a vocalization peak between 20:00 h and 21:00 h. Its vocalization activity was related to total precipitation. The nests, composed by only one folded leaf, are placed on shrubs along streams. The nests, which hang over the stream pools, contain approximately 30 eggs that last about 13 days of incubation, producing about 25 tadpoles per spawning. Males are territorial, remaining in the same places for more than 60 days, defending them through vocalizations and eventual physical combats. Males with a higher body condition usually stay longer in the same territory. We also recorded males displaying satellite behavior. ARTICLE HISTORY
