Fused Testes in Neotropical Frogs of the Genus Pristimantis (Anura, Craugastoridae): New Insights Into a Poorly Known Character in Vertebrates

Abstract

Amphibian testes vary in shape, from multilobed in caecilians and salamanders to compact, ovoid organs in anurans. Although these variations have been studied extensively in amphibians, there has been little investigation into the structural, copulatory, and reproductive behavioral consequences of unpaired testes, a character shared among some amphibians, cyclostomates, and some teleosts. We analyzed the morphology and structure of unpaired testes in Pristimantis fetosus and Pristimantis permixtus. We also report a single testis in P. hernandezi. Our results suggest that the testis arrangement in these species results from the hypertrophy and fusion of two testes rather than the loss or reduction of one testis. Furthermore, the occurrence of germ cells at different stages of development suggests that spermatogenesis is similar to that described for vertebrates, with spermatogonia undergoing mitosis to form spermatocytes, which then undergo meiosis to form spermatids. Like other brachycephaloid frogs, Pristimantis with fused testes exhibit direct development and reproduction on land, but they are the only anurans known to undergo testicular fusion. We propose to recognize the occurrence of fused testes as a unique putative synapomorphy for a new species group distributed in the Colombian Andes, which we refer to as the P. hernandezi species group. A comparative survey among vertebrates reveals no apparent variations in testicular organization, sperm development, or copulative and reproductive behavioral characters associated with the fusion of testes, suggesting that its occurrence might not have functional implications for vertebrate testes. The independently evolved occurrence of fused testes in cyclostomates, teleosts, and amphibians raises an exciting perspective on the study of the molecular origin, evolution, and functional significance of testis variation in vertebrate reproduction and biology.