Transmissible cancer and the evolution of sex.

Frédéric Thomas,Beata Ujvari,Orsolya Vincze,Benjamin Roche,François Renaud,Mathieu Giraudeau,Rodrigo Hamede,Thomas Madsen,Dorothée Misse

doi:10.1371/journal.pbio.3000275

Abstract

The origin and subsequent maintenance of sex and recombination are among the most elusive and controversial problems in evolutionary biology. Here, we propose a novel hypothesis, suggesting that sexual reproduction not only evolved to reduce the negative effects of the accumulation of deleterious mutations and processes associated with pathogen and/or parasite resistance but also to prevent invasion by transmissible selfish neoplastic cheater cells, henceforth referred to as transmissible cancer cells. Sexual reproduction permits systematic change of the multicellular organism’s genotype and hence an enhanced detection of transmissible cancer cells by immune system. Given the omnipresence of oncogenic processes in multicellular organisms, together with the fact that transmissible cancer cells can have dramatic effects on their host fitness, our scenario suggests that the benefits of sex and concomitant recombination will be large and permanent, explaining why sexual reproduction is, despite its costs, the dominant mode of reproduction among eukaryotes.

Highlights

Because clonal reproduction leads to organisms that are identical, we propose that (1) malignant cells produced by the first multicellular organisms were likely to be well adapted to other organisms, including direct descendants; (2) it was difficult for the victim organisms to recognize transmissible cancer cells that were almost identical to normal somatic cells
If the transmission of cancerous cells was a major factor in the evolution of sexual reproduction, the negative effects of such cheaters may affect “super organisms,” such as social insect colonies, the queen being the gonads, the workers being the somatic cells, a system comparable to that of a multicellular organism [34]
A major constraint of such transmissions requires an ability of transmissible cancerous cells to evade immunological histocompatibility barriers

Summary

Introduction

The first asexual multicellular organisms did have to deal with their own cheater cells and to evolve adaptations preventing the colonization by infectious malignant cells coming from other individuals. Because clonal reproduction leads to organisms that are identical, we propose that (1) malignant cells produced by the first multicellular organisms were likely to be well adapted to other (identical) organisms, including direct descendants; (2) it was difficult for the victim organisms to recognize (and eliminate) transmissible cancer cells that were almost identical to normal somatic cells (i.e., immune evasion).

Results

Conclusion