Sexual selection, genetic conflict, selfish genes, and the atypical patterns of gene expression in spermatogenic cells

Abstract

This review proposes that the peculiar patterns of gene expression in spermatogenic cells are the consequence of powerful evolutionary forces known as sexual selection. Sexual selection is generally characterized by intense competition of males for females, an enormous variety of the strategies to maximize male reproductive success, exaggerated male traits at all levels of biological organization, co-evolution of sexual traits in males and females, and conflict between the sexual advantage of the male trait and the reproductive fitness of females and the individual fitness of both sexes. In addition, spermatogenesis is afflicted by selfish genes that promote their transmission to progeny while causing deleterious effects. Sexual selection, selfish genes, and genetic conflict provide compelling explanations for many atypical features of gene expression in spermatogenic cells including the gross overexpression of certain mRNAs, transcripts encoding truncated proteins that cannot carry out basic functions of the proteins encoded by the same genes in somatic cells, the large number of gene families containing paralogous genes encoding spermatogenic cell-specific isoforms, the large number of testis-cancer-associated genes that are expressed only in spermatogenic cells and malignant cells, and the overbearing role of Sertoli cells in regulating the number and quality of spermatozoa.

Evolutionary biology of cancer

“…Recently, a suite of genes involved in carcinogenesis have been shown to exhibit signatures of positive selection [44][45][46] and, in each case, this selection appears to involve evolutionary antagonisms, such as those seen in parent-offspring conflict, sexual conflict, sexually selected conflict or intragenomic conflict [46][47][48].…”

“…Kleene [47] describes how intragenomic conflict and sexual selection might both characterize genes involved in spermatogenesis, and that many of these genes promote rapid cell replication and exhibit unusual patterns of expression (such as dramatic overexpression) in cells involved in spermatogenesis and in malignant cells. Indeed, a whole suite of 'cancer-testis-associated (CTA) genes' is expressed only in the testes and malignant cells [47], and some of these genes have been subject to strong positive selection among species.…”

“…Indeed, a whole suite of 'cancer-testis-associated (CTA) genes' is expressed only in the testes and malignant cells [47], and some of these genes have been subject to strong positive selection among species. Thus, genetic pathways involving CTA genes, which evolved in the context of sexual conflict and sexual selection, are apparently coopted by cancer cell lineages during somatic evolution, as developing cancer cells avoid apoptosis, dedifferentiate and take on properties of immortal male germ cells (5,46,47).…”

“…The hunt for genes related to cancer could be accelerated by evaluating for cancer-risk genes that have been subject to rapid evolution along the human lineage, with special emphasis on those that are expressed during gamete, embryonic and placental development [46,47,51]. Such genes, and known oncogenes and tumor suppressors, should also be sequenced in a much wider range of primates and other mammals, to identify positively selected amino acid sites and link adaptive molecular evolution to aspects of life history and mating systems.…”

“…Comparative viewpoints on cancer also lead directly to concerns that animal models, such as mice, have less applicability to humans than is currently believed, because anticancer adaptations should be more or less unique to each species [60] and artificial selection inadvertently applied to laboratory animals has fundamentally altered their physiology and life history [41,84]. cancer from computer to laboratory to clinic (Box 3), analyses of how cancer evolves should also provide novel insights into outstanding questions in evolutionary ecology [43,47,48,55,63,66]. Only through integrated molecular, ecological and evolutionary analyses of cancer, at the somatic, population and macroevolutionary levels, will we come to understand and govern this unique disease.…”