Phenotypic plasticity and social life facilitate the evolution of new phenotypes in ants – ANTEVO

We collect colonies of two ant genera (Mystrium et Temnothorax). First, we study morphology, physiology and behavior of developmental anomalies produced naturally or artificially in colonies. Second, we describe development and gene expression of larvae of novel wingless queen castes. Using a comparative approach, we propose that novel castes evolved from developmental anomalies.

Some colonies possess a few anomalies. The first results on Mystrium show that they are mosaics that combine queen and worker traits, they survive and work in colonies, and they can become reproductively active. We develop probes to detect gene expression in larvae and methods for dissection and histology, in order to test whether wingless queens are mosaics as well.

The first results confirm our hypotheses. Instead of producing true novelties, ants can produce mosaics of winged queens and workers. These mosaics survive, as they are protected by nestmates, and they can bring benefits to the whole colony. They could be selected and evolve into new mosaic castes such as wingless queens. This mechanism could accelerate ant evolution and it may have contributed to ant biodiversity.

These results will be presented during the French meeting of the International Union for the Study of Social Insects in August 2013 in Villetaneuse, with two conferences and one poster. The results about Mystrium anomalies will lead to the redaction of two or three manuscripts from September 2013.

Studying the mechanisms that allow for the production, survival and selection of novel phenotypes is crucial to understand biodiversity and evolution. Phenotypic plasticity has recently been considered as a factor favouring the production of novel phenotypes after environmental changes. In polyphenic organisms, i.e. exhibiting phenotypic plasticity with discrete alternative forms (e.g. butterfly seasonal morphs), novel phenotypes can be generated by combining traits expressed in alternative phenotypes. The occurrence of such new phenotypes is often observed at very low frequency and their production can be increased after environmental changes. We propose that new phenotypes are more likely to occur and to be favoured by selection in polyphenic social species, and that this enhanced potential for evolving new morphologies may affect how they will react to global changes.
Ants are an ideal model to study the evolution of new phenotypes. They are highly polyphenic with two markedly distinct castes: winged queens specialize in colony founding and egg-laying while wingless workers perform all other tasks. These two adult phenotypes are generally environmentally-determined during larval development. Many ant species produce novel castes in addition to (or in replacement of) these ancestral queens and workers castes, including wingless queens and soldiers. Novel castes evolved independently numerous times, and we propose to study how ants can so readily evolve them. Central to our thinking is the erratic production of anomalous phenotypes which are intermediate between queens and workers (intercastes), and which we hypothesise to be the origin of new phenotypes. We will address three questions.
First, we will investigate whether environmental changes (temperature) and hormonal treatments affect the rate of production of intercastes. Using morphometrics we will compare their phenotypes with the regular castes (worker and winged queen) and naturally-occurring intercastes. Second, we will test whether intercastes and novel castes (wingless queens and soldiers) are produced by recombining developmental modules from existing winged queens and wingless workers. Using in-situ hybridization we will study gene expression in larval imaginal discs to test our prediction that the gene networks expressed in wingless queens and soldiers are not modified de novo but recycled from the ancestral worker and winged queen castes. Third, using ethological, morphometric and dissection methods, we will test the hypotheses that novel phenotypes are shielded from individual selection in social taxa and that they may yield colony-level benefits. New phenotypes are more likely to survive in social than in solitary species because the colony buffers them against the outside environment (colonial buffering hypothesis), and their production could bring colony-level benefits when their new morphologies, combined with the division of labour that characterises social insects, make them more efficient at performing certain tasks (usefulness of certain intercastes hypothesis). We will also compare intercastes with the regular wingless queen and soldier castes in order to discuss their evolution.
Testing these hypotheses for the evolution of novel phenotypes can help a better understanding of the spectacular evolution of morphological diversity in ants and of the evolution of biodiversity in general, as well as whether phenotypic plasticity may facilitate adaptations to global changes.