American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Experimental evidence that metamorphosis alleviates genomic conflict”

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Debora Goedert and Ryan Calsbeek (Sep 2019)

Read the Article (Just Accepted)

Metamorphosis changes integration between traits and alleviates ontogenetic conflict across amphibian life stages

Wood frog juvenile in the final stage of metamorphosis.<br />(Credit: Debora Goedert)
Wood frog juvenile in the final stage of metamorphosis.
(Credit: Debora Goedert)

Metamorphosis is a remarkable characteristic of many amphibians, marking the transition from an aquatic to a terrestrial life stage. Metamorphosis is a complex and costly process and the benefits of metamorphosis have long puzzled biologists. One possibility is that the morphological changes that occur during metamorphosis allow natural selection to shape the two life stages independently of each other in their respective habitats. Given that tadpoles and frogs are life stages of a single individual, and must be formed from the same genetic material, one might wonder whether it is possible to adapt to one environment without paying a cost of adaptation in the other.

In this study, Goedert and Calsbeek use wood frogs to investigate the so-called ‘adaptive decoupling hypothesis’. The researchers performed controlled mattings in the laboratory and reared hundreds of tadpoles through metamorphosis. Their breeding design allowed them to test for patterns of integration in the inheritance of tadpole and frog morphology – for instance, the researchers were able to ask whether having genes for a long tail as a tadpole would lead to long legged frogs. They showed that, although there is some genetic integration between tadpole and frog morphologies, the degree of such integration was much lower between life stages than within either tadpoles or frogs. This study provides some of the first evidence that metamorphosis may have evolved to allow natural selection to shape a single genome into two very different life forms.


Abstract

Whenever genetically correlated traits experience antagonistic selection, an adaptive response in one trait can lead to a maladaptive response in the correlated trait. This is a form of genome-level conflict that can have important evolutionary consequences by impeding organisms from reaching their adaptive optima. Antagonistic selection should be pervasive in organisms with complex life histories because larval and adult life stages specialize in dramatically different environments. Since individuals express larval and adult morphologies from a single genome, genomic conflict across ontogenetic stages should also be prevalent. Using wood frogs as a study system, we measured natural selection on larval and post-metamorphic life stages, and estimated genetic correlations among traits. Alternative life stages experienced a mix of both antagonistic and congruent viability selection. The integration between traits changed over the course of metamorphosis, reducing genetic correlations that cause conflict. Our results provide novel experimental evidence that metamorphosis can alleviate genomic conflict by partitioning life history stages into modules that can more readily respond to selection. These results highlight the adaptive potential of metamorphosis as a means to avoid ecological specialization trade-offs. Moreover, they provide insights into the prevalence and evolutionary maintenance of complex life cycles.

Evidência experimental de que a metamorfose reduz conflito genômico

Quando pressões seletivas antagonistas atuam em características geneticamente correlacionadas, a resposta adaptativa de uma dessas características pode resultar em uma resposta maladaptativa na característica correlacionada. Tal situação representa uma forma de conflito genômico que pode ter importantes consequências evolutivas ao impedir organismos de atingir seu valor adaptativo máximo. Espera-se que seleção antagonista seja comum em organismos com ciclo de vida complexos, porque estágios larvais e adultos são especialistas em ambientes muito diferentes. Além disso, como indivíduos expressam morfologias de larva e adulto utilizando um mesmo genoma, o conflito genômico entre esses estágios ontogenéticos deve ser prevalente. Usando sapos (Rana sylvatica) como organismo modelo, medimos seleção natural tanto no estágio larval quanto em estágios pós-metamorfose, e estimamos correlações genéticas entre características de ambos estágios. Os diferentes estágios ontogenéticos apresentaram uma combinação de seleção de viabilidade em direções antagonistas e congruentes. O nível de integração entre características variou ao longo do processo de metamorfose, havendo redução de correlações genéticas que poderiam causar conflito genômico. Nossos resultados demostram evidência de que o processo de metamorfose pode aliviar o conflito genômico ao particionar os estágios ontogenéticos em módulos, permitindo que estes respondam mais rapidamente a forças seletivas. Esses resultados enfatizam o potencial adaptativo da metamorfose como uma forma de evitar demandas conflitantes durante especialização ecológica dos estágios de vida. Mais ainda, esses resultados contribuem para o entendimento da prevalência e manutenção evolutiva de ciclos de vida complexos.