Monday 12 March 2018

Earless Frogs and Their Unique Habitats – via Herp Digest


National Geographic Blog 3/7/18 by Scott Ridge 

Rudolf von May, a National Geographic Society grantee, studied habitat shifts and physiology of ground-breeding frogs across Andes-Amazon elevational gradients. Last month, von May’s research paper, “Evolutionary radiation of earless frogs in the Andes: molecular phylogenetics and habitat shifts in high-elevation terrestrial breeding frogs” was published in PeerJ, a leading open access peer-reviewed scientific journal. We asked Dr. von May about his findings.

You studied terrestrial breeding frogs living at high elevations in the Andes, specifically earless frogs. What is an earless frog and how many other species of frog are similar? What some of the key findings in your research?

Earless frogs are those that lack a tympanum, which is visible as an eardrum surrounded by a ring of cartilage in most eared frogs. More specifically, the eardrum is called tympanic membrane, the ring is called tympanic annulus, and both are part of the tympanic middle ear, which also includes a bone called columella. Altogether, these structures aid in the transmission of airborne sound to the inner ear.

The amphibian tree of life contains hundreds of species of earless frogs. The most prominent example includes those in the true toad family, Bufonidae, which has approximately 200 earless species out of a total of 609 known species. The loss of hearing structures has occurred multiple times in this and other amphibian families. However, in most cases, male earless frogs have retained the ability to call and species evolved alternative sensory pathways that enable the transmission of sound to the inner ear. For example, the earless Gardiner’s Seychelles Frog (endemic to the Seychelles) use the mouth cavity as a resonating chamber to amplify the sound and transmit it to the inner ear.

The Andean frog genus Phrynopus [see photos] represents a special case where the large majority of species (>90%) have lost the tympanic membrane and tympanic annulus, and we have identified a single evolutionary event that involved the loss of both structures and that appears to have predated the increase of species diversity in this group. We also observed that the loss of hearing structures is correlated with the absence of advertisement calls. This is interesting because, although the loss of hearing structures has occurred multiple times throughout the evolutionary history of frogs, the existence of earless frogs that do not produce advertisement calls is far less common.

Can you explain evolutionary radiation and how it related to the species of frogs you studied?
An evolutionary radiation is the process by which many species evolve from a common ancestor, resulting in an increase of species diversity through time. This increase in species diversity is often correlated with morphological changes and the colonization of new habitats.
The frogs we studied belong to a large family of land-breeding or terrestrial-breeding frogs called Strabomantidae. Terrestrial breeding frogs have undergone an extraordinary evolutionary radiation that resulted in nearly 700 species. These frogs use a specialized reproductive mode called direct development in which embryos hatch directly into froglets (i.e., there are no free-living tadpoles) — a strategy that allows the group to exploit a wide variety of habitats, as long as those habitats contain sufficient moisture. We were interested in studying this group because a recurrent theme is the loss of hearing structures and loss of advertisement calls.

Your findings show an “absence of advertisement calls.” Can you explain further and why it’s important to understand in breeding frogs?
Advertisement calls are the main form of acoustic signal used by male frogs to attract potential mates. As such, advertisement calls are recognized as a premating isolation mechanism. Speciation in the absence of common acoustic signals and the associated sensory system in frogs, such as the one observed in Phrynopus, raises questions about the factors that affect speciation. Why frogs lost their ear and why they don’t call are questions that remain elusive, and motivate further scientific research.
What role does high elevation play in the biology of these frogs?
We found that species’ phenotype changes with elevation. Specifically, we detected a significant pattern of increasing body size with increasing elevation, and that species at higher elevations tend to develop shorter limbs, shorter head, and shorter snout than species living at lower elevations. Our findings strongly suggest a link between ecological divergence and morphological diversity of terrestrial breeding frogs living in montane gradients.
PHRYNOPUS PERUANUS FOUND IN ANDEAN GRASSLAND IN PERU. (PHOTOGRAPH BY RUDOLF VON MAY)

How did you collect the data in your research and what technology was crucial in your work?
My colleague Edgar Lehr and I conducted several field expeditions between 2012 and 2014, in a region where mountains taller than 13,000 feet are common. We collected ecological data, museum specimens, and DNA sequence data that were used to build an evolutionary tree for the current study. Some of our fieldwork was carried out in collaboration with other colleagues from Peru and the Czech Republic, an included the participation of local guides who provided invaluable help in the field. Also, when we surveyed protected areas, we worked with the park administration and several rangers.

We used standard laboratory methods including polymerase chain reaction (PCR) and a Sequence Analyzer to obtain DNA sequences that we then included in molecular phylogenetic analyses to infer an evolutionary tree for the species under study. The resulting phylogenetic tree was used to perform different analyses that took into account the phylogenetic relatedness (or evolutionary relatedness) among species. For example, we mapped the tympanum condition on to the evolutionary tree to identify a single evolutionary transition that involved the loss of both the tympanic membrane and tympanic annulus. Our phylogenetic analysis also resulted in the discovery of new species such as Phrynopus inti [see photo on top of page], described in 2017.

We used X-ray computed tomography (CT) imaging to test if the absence of external hearing structures is associated with the loss of the auditory skeletal elements such as the columella (also known as stapes; see image below). Our analysis demonstrated that the absence of tympanum is associated with complete loss of columella in at least one member of the genus.

COURTESY OF RUDOLF VON MAY AND ERIN WESTEEN

What would you like teachers and students to know about the work you and your team did in South America?
The number of known frog species in the world continues to increase as a result of new discoveries and descriptions (on average, between 100 and 200 new species are described per year). In the Andean genus Phrynopus, about one third of the currently known species (34) were described over the past decade; only in 2017 alone, seven new species of Phrynopus were described. The discovery of new species demonstrates the need for further scientific exploration of poorly known areas in South America, as these areas often contain unique habitats and species living in them.

Study coauthors are Edgar Lehr, Professor at Illinois Wesleyan University, and Daniel Rabosky, Assistant Professor at the University of Michigan (Museum of Zoology and the Department of Ecology and Evolutionary Biology). The study received financial support from the National Geographic Society, the National Science Foundation, the David and Lucile Packard Foundation, and several other organizations. Research permits and logistical support were provided by Peru’s wildlife service (SERFOR) and the national park service (SERNANP).

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