Molecular ‘fossils’ reveal evolutionary history of descending testicles

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Conventional fossils reveal an animal's bones, but not soft body parts. A new study shows how "molecular fossils" can reveal whether the testicles of long-dead mammals descended into the lower abdomen or scrotums, or were retained deep inside the abdomen. The study, publishing 28 June in the open access journal PLOS Biology by Virag Sharma and Michael Hiller of the Max Planck Institute of Molecular Cell Biology and Genetics in Dresden, Germany, and colleagues, shows that the testicles of the ancestor of all placental mammals would have descended during development, and that the retention of testicles in a group of modern African mammals is due to specific gene changes relatively late in evolution.

Testicular descent during development serves to position the testicles so they can be cooler than the rest of the body, which is important for sperm maturation. But in one group of mammals — the Afrotherians, which includes manatees, elephants, and several small insectivores — the testicles do not descend, and are instead retained deep inside the abdomen throughout adulthood. Because, like most other soft tissues, the testicles are not preserved in the fossil record, it has been unclear whether the testicles of the common ancestor of all mammals descended or were retained.

To explore this question, the authors analyzed the genomes of 71 placental mammalian species, focusing on two key genes (RXFP2 and INSL3) that are known to induce the development of the gubernaculum, a ligament that helps pull the testes downward during development. They found that these two genes were either lost or completely nonfunctional in four Afrotherian species (tenrec, cape elephant shrew, cape golden mole, and manatee), and that these gene losses happened after the Afrotherian group split from the ancestral placental mammal about 100 million years ago. The inactivating mutations differed among the four evolutionary lineages, further suggesting that the molecular causes of retention are more recent (20-80 million years ago) and independent, rather than ancestral and shared, in these species. The two genes appeared to be functional in two other Afrotherian species (elephants and rock hyrax), and the causes of their testicular retention remain unknown.

Beyond solving a specific riddle in mammalian evolution, the examination of the vestiges of soft-tissue genes may have very broad applicability in reconstructing changes in body parts and developmental processes through evolutionary time, says Hiller. "Molecular vestiges offer an alternative strategy to investigate character ancestry. Instead of investigating a soft-tissue structure directly, one can trace the evolution of genes that are crucial for the development of this structure."

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In your coverage please use this URL to provide access to the freely available article in PLOS Biology: http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.2005293

Citation: Sharma V, Lehmann T, Stuckas H, Funke L, Hiller M (2018) Loss of RXFP2 and INSL3 genes in Afrotheria shows that testicular descent is the ancestral condition in placental mammals. PLoS Biol 16(6): e2005293. https://doi.org/10.1371/journal.pbio.2005293

Funding: Max Planck Society. Received by MH. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. German Research Foundation (grant number HI 1423/3-1). Received by MH. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Leibniz Association (grant number SAW-2016-SGN-2). Received by TL, HS, MH. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing Interests: The authors have declared that no competing interests exist.

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       <h4>Related Journal Article</h4>http://dx.doi.org/10.1371/journal.pbio.2005293 
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