Reproductive Mode Evolution

amphibians, comparative phylogenetics, life-history traits


The majority of species in the animal kingdom have complex life cycles. That is, their ontogenetic development from embryo to adult is not a continuous process, but rather is broken up into distinct ontogenetic phases. Typically, one or more larval phases and an adult phase, separated by short periods of extensive remodelling of the body plan (metamorphosis). However, major branches on the tree of life, such as the amniotes, have lost the larval stage to exhibit a simplified, uniphasic life cycle. How this has come about is a fundamental evolutionary question. This same loss has occurred frequently in anamniotes, perhaps most prominently so in Amphibia. Moreover, amphibians have experienced extensive evolutionary modifications to their ancestral, biphasic life cycle. Over the > 350 million years since their origin, they have evolved an impressive repertoire of embryonic and larval developmental alternatives including both loss of larval stages (direct development or viviparity) and loss of the adult stage (paedomorphosis). This makes amphibians and interesting system for studying how major transitions in life history can evolve.

Evolution of Reproductive Modes in Amphibians

Much of the diversity in life histories in amphibians involves the presence or absence of whole life stages and on whether embryonic and larval development occurs in water or on land. These two aspects are often tightly linked. For example, most oviparous species that have lost the larval stage (direct development) lay terrestrial eggs. Amphibian life-histories are thus traditionally thought of as having evolved sequentially with only single ontogenetic modules (life stages) changing at each point in time. According to this sequential view, biphasic, fully aquatic development is thought to be ancestral. The evolution of a terrestrial egg, but with an aquatic larval stage represents the first step in this sequence. The evolution of a terrestrial larval stage then followed, before losing the larval stage completely to become direct developing (i.e. post-metamorphic juveniles hatching from eggs). Live-bearing would then be the most derived mode, in which embryos are retained (with or without the egg) in the oviduct of the mother up until metamorphosis, or in some cases, late stages of larval development.

There is evidence both for and against this “sequential” view of how reproductive modes and terrestriality have evolved. We are interested in using the most current phylogenetic comparative methods to test this idea.

The results of this project are published in Nature Communications.

Terrestrial reproductive modes are correlated with steep, tropical terrain

A longstanding question in vertebrate biology has been the evolution of terres- trial life histories in amphibians and here, by investigating African bufonids, we test whether terrestrial modes of reproduction have evolved as adaptations to particular abiotic habitat parameters. We reconstruct and date the most complete species-level molecular phylogeny and estimate ancestral states for reproductive modes. By correlating continuous habitat measurements from remote sensing data and locality records with life-history transitions, we dis- cover that terrestrial modes of reproduction, including viviparity evolved multiple times in this group, most often directly from fully aquatic modes. Terrestrial modes of reproduction are strongly correlated with steep terrain and low availability of accumulated water sources. Evolutionary transitions to terrestrial modes of reproduction occurred synchronously with or after transitions in habitat, and we, therefore, interpret terrestrial breeding as an adaptation to these abiotic conditions, rather than an exaptation that facilitated the colonization of montane habitats.

The results of this project are published in Proceedings of the Royal Society B.

Tropical montain forests as an evolutionary breeding ground for terrestrial reproductive modes

Using a dataset that comprises 180 amphibian species from various East African habitats, we tested whether species occurring in different habitats show different patterns of terrestrialization in their breeding strategy. We recovered a significant association between terrestrialized breeding strategies and forest habitats. In general, forest seems to act as a facilitator, providing a permissive environment for the evolution of terrestrialized breeding strategies. However, while terrestrial oviposition is strongly correlated with lowland and montane forest habitat, complete terrestrial development is significantly correlated with montane forest only, indicating different selective pressures acting at different steps towards complete terrestrial development.

The results of this project are published in Biology Letters.

[amphibians comparative phylogenetics life-history traits]
Simon Loader, Hendrik Müller, Ivan Gomez-Mestre, John J. Wiens
May 1, 2024