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research REFLECTIONS FROM HARRY GREENE

Show me you care: female mate choice based on egg attendance rather than male or territorial traits
April 29, 2021

Male Amazonian Glass Frog (Hyalinobatrachium cappellei) on the underside of a leaf, vocalizing to attract females while attending to a clutch of eggs. Image credit: Anyelet Valencia-Aguilar

REFLECTION BY HARRY GREENE:

Article Details:

Citation:

Valencia-Aguilar, A., K. R. Zamudio, C. F. B. Haddad, S. M. Bogdanowicz, and C. P. A. Prado. Show me you care: female mate choice based on egg attendance rather than male or territorial traits. Behavioral Ecology 31:1054-1064.

In the 1980s, as a young Berkeley professor, I began promoting natural history research and teaching, activities that focus on how organisms are built and make their livings, the specifics of their surroundings and so forth. Back then, as is still true, natural history was threatened by poor financial support, elimination of college courses about flora and fauna, fewer outlets for publishing, and the growing appeal of technology for its own sake. Because “cell-smashers” and “gel jocks” were, in my view, getting way too much money and glory, I railed against them in book reviews, essays, and lectures. Fast forward 40 years and I am so over that hostility! Now biologists of all stripes realize that microbes, plants, and animals themselves yield our most interesting questions, yet just as surely genomics offers answers not even imagined 40 years ago. Indeed, this posting’s featured paper was unimaginable back then, because there was no basis for suspecting female glass frogs (Centrolenidae) would choose mates based upon male parenting skills.

I’d earned a 1977 Ph.D. in ethology, which emphasizes studying behavior in nature. My focus since childhood had been amphibians and reptiles, and whatever they seemingly lacked in social and cognitive complexity was more than balanced by their spectacular diversity. Frogs, for example, were ancestrally terrestrial jumpers, yet span thousands of species of diggers, swimmers, climbers, and gliders. Turns out, too, that their breeding habits are far more complex than was realized in my youth—case in point, the eggs of Darwin’s Frogs are ingested by males, development takes place in his paired vocal sacs, and fully-formed froglets are coughed up by their fathers. Frogs are also super charismatic, arguably none more so than centrolenids. Distributed from Mexico to Argentina, these bug-eyed living emeralds have translucent under-surfaces through which organs, blood vessels, and blue-green bones often are visible. Temperate amphibians typically depart aquatic breeding sites immediately after laying eggs, but glass frogs oviposit on foliage over streams and have repeatedly evolved paternal care.

Lead author Anyelet Valencia-Aguilar in her southern Amazonian study site, Mato Grosso, Brazil. Image credit: Anyelet Valencia-Aguilar

Enter Anyelet Valencia-Aguilar, working for her Ph.D. in Brazil, supervised by Cynthia Prado and Celio Haddad, the three of them collaborating with Kelly Zamudio and Steve Bogdanowicz of Cornell University. Anyelet had studied glass frogs as a Colombian undergraduate and wanted to further explore why males exhibit parental care. Kelly’s doctoral dissertation focused on lizard life history evolution, but upon moving to a professorship in NY she adopted molecular genetic techniques to reveal that female salamanders choose mates based on traits like body mass. Together they now would use similar approaches to better understand glass frogs. The resulting fieldwork was epic, the lab procedures complicated, but by sampling DNA from adults and offspring with known behavioral histories the researchers could assess the parentage of particular egg clutches.

Having visited Anyelet’s study site with Kelly and Cynthia, I’ve never been more impressed with how much effort, paper by published paper, underlies our knowledge of organisms—even single sentences in field guides and textbooks may summarize the lifetime efforts of several natural historians. Getting to Fazenda São Nicolau meant flying to the end of the line in southern Amazonia, ten hours on roads that were sometimes no more than muddy two-tracks, and a mesmerizing 20-minute ferry ride across the Rio Juruena. Fieldwork was mostly at night, amidst jaguars, peccaries, tapirs, caimans, snakes, and a plethora of stinging and biting insects. Along three streams, twice daily over the course of two successive breeding seasons, Anyelet observed glass frogs, often from a ladder high above the rainforest floor. She mapped nesting sites and filmed male-male and female-male interactions; she recorded egg mass characteristics and hung plastic containers under clutches to collect hatching larvae. Next came months of tedious pipetting, gene sequencing, and computer analyses at Cornell, then the writing, editing, and prepublication review process.

All that field and lab time boiled down to 11 printed pages in a premier scientific journal. Paraphrasing from the paper, female glass frogs did not select for male body condition, calling persistence, or habitat traits; instead, they chose mates who were sitting with pre-existing clutches. Males actively cared only for their own offspring—rotating eggs with their hands and feet to clean them, thereby preventing fungal infections—but they increased mating opportunities by remaining near clutches fertilized by other males. Withal, these are just the sorts of unexpected discoveries that change our generalizations about how life works and evolves. They also inspire appreciation for nature. I hope readers will enjoy this publication, pause to savor its Figure 1, and like me fall in love with glass frogs.

 

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Meet Harry Greene

Harry W. Greene is emeritus professor of ecology and evolutionary biology at Cornell University, author of Snakes: The Evolution of Mystery in Nature and Tracks and Shadows: Field Biology as Art, and a member of the NHI’s science advisory council.

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