Reproductive mode plasticity: Aquatic and terrestrial oviposition in a treefrog

Abstract

Diversification of reproductive mode is a major theme in animal evolution. Vertebrate reproduction began in water, and terrestrial eggs evolved multiple times in fishes and amphibians and in the amniote ancestor. Because oxygen uptake from water conflicts with water retention in air, egg adaptations to one environment typically preclude development in the other. Few animals have variable reproductive modes, and no vertebrates are known to lay eggs both in water and on land. We report phenotypic plasticity of reproduction with aquatic and terrestrial egg deposition by a frog. The treefrog Dendropsophus ebraccatus, known to lay eggs terrestrially, also lays eggs in water, both at the surface and fully submerged, and chooses its reproductive mode based on the shade above a pond. Under unshaded conditions, in a disturbed habitat and in experimental mesocosms, these frogs lay most of their egg masses aquatically. The same pairs also can lay eggs terrestrially, on vegetation over water, even during a single night. Eggs can survive in both aquatic and terrestrial environments, and variable mortality risks in each may make oviposition plasticity adaptive. Phylogenetically, D. ebraccatus branches from the basal node in a clade of terrestrially breeding species, nested within a larger lineage of aquatic-breeding frogs. Reproductive plasticity in D. ebraccatus may represent a retained ancestral state intermediate in the evolution of terrestrial reproduction.aquatic egg-laying ͉ evolution of reproductive mode ͉ Hyla ebraccata ͉ phenotypic plasticity ͉ climate change T he evolution of terrestrially developing eggs from ancestral aquatic eggs is a repeated trend in both invertebrates and vertebrates (1-10). In both groups, aquatic predators and constraints on oxygen uptake are hypothesized to select for terrestrial eggs (2, 7-11). Terrestrial eggs can improve the embryonic respiratory environment, allow oviposition over fast-moving streams where aquatic eggs might be swept away, and allow animals to colonize habitats without permanent water bodies (2, 4, 7-10). However, terrestrial eggs experience new risks from desiccation and terrestrial predators (2, 4, 7-10). Because aquatic and terrestrial environments select for different traits, eggs are usually well adapted to only one environment (2, 4). Adaptations for terrestrial oviposition have evolved independently in several groups [e.g., gastropods (8, 12), insects (9, 13), and fishes and amphibians (1, 2, 4, 10)]. In all of these organisms, the divergence in reproductive mode [oviposition site and type of egg development (1, 2, 10)] occurred long ago, and it is thus difficult to directly assess selective pressures that may have influenced such evolution. Closely related species or populations that vary in their reproductive modes [e.g., between viviparity and oviparity (14-18)] offer the best opportunity to study the selective pressures leading to reproductive mode diversification. Although some foam-nesting frogs are reported to place nests in diverse locations (10,19,20), t...

Species composition and reproductive modes of anurans from a transitional Amazonian forest, Brazil

“…However, it is also possible to observe reproductive plasticity in amphibians that do not succumb in the face of environmental changes, for instance Dendropsophus ebraccatus (Cope, 1874). This species can lay eggs both in water bodies and on terrestrial habitats, depending on environmental conditions, and select oviposition sites in response to factors that can promote egg desiccation (TOUCHON & WARKENTIN 2008).…”

An unusual reproductive mode in Hypsiboas (Anura: Hylidae)

“…For example, species that construct basins in which eggs are laid (mode 4), essentially do not differ in any way in their egg and larval development from many anurans with mode 1. Consequently, they sometimes will place eggs in natural rock pools or streams (WELLS 2007). This was already verified for the nest-building gladiator frog H. faber by HADDAD & PRADO (2005).…”

“…The plasticity of reproductive modes is rarely reported, perhaps because it has been considered a fixed behavior (TOUCHON & WARKENTIN 2008). For example, species that construct basins in which eggs are laid (mode 4), essentially do not differ in any way in their egg and larval development from many anurans with mode 1.…”

“…Natural variation in oviposition sites may reflect plasticity in the behavioral response of anurans to different environment conditions (WELLS 2007, TOUCHON & WARKENTIN 2008. The plasticity of reproductive modes is rarely reported, perhaps because it has been considered a fixed behavior (TOUCHON & WARKENTIN 2008).…”

Oviposition site choice under conflicting risks demonstrates that aquatic predators drive terrestrial egg-laying

“…The pantless treefrog, Dendropsophus ebraccatus [40], provides a unique opportunity to use oviposition site choice to evaluate the importance of various selective agents on terrestrial reproduction because this species has plasticity in its reproductive mode, flexibly laying either aquatic or arboreal eggs in different environmental contexts [41,42]. We refer to the non-aquatic eggs of D. ebraccatus as 'arboreal' to avoid confusion with direct-developing anuran eggs, which are often referred to as 'terrestrial'.…”