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You are the result of what your ancestors survived

Hormones trade size for survival in warming climates...

All over the world, toad species are managing to survive warmer and drier climates. Now, researchers at the University of Cincinnati believe they know how they manage to alter their developmental timetable and adapt.

University of Cincinnati (UC) associate professor Daniel Buchholz PhD, biologist on the study, credits survival of spadefoot toads to a theory of hereditary change called "genetic accommodation" — evolution that happens in response to a changing environment.

Recently published in Nature Communications, the research explains how some spadefoot tadpoles metamorphosis is controlled by hormone changes reacting over time to environmental changes such as temperature and humidity. Called "phenotypic plasticity" it means the ability to change physical characteristics in an animal (or plant or microbe).

Explains Buchholz: "We found that when certain species combined stress hormones produced by the adrenal gland with hormones produced in the thyroid gland, this was key in speeding their development and shortening the larval periods. This process helps assure that they metamorphose or hatch before the pond dries up."

Researchers traveled the world to find and collect the three species of spadefoot toads that reflected phenotypic plasticity, one from Doñana, Spain and two different species from Arizona, USA. In experiments at UC, Buchholz and Saurabh Kulkarni, UC biology graduate student and first author, the larval stages of each species were compared to each other as they matured without outside environmental influence. The Spanish and American species, indigenous to permanent and semipermanent pond life, had more flexible control over their development as they activated metamorphosis upon perceiving their pond habitat was drying.

However, the desert Scaphiopus couchii toad, from the American southwest, already had the shortest larval period of the three. More than likely a response to the gradual drying out of the southwest since the 1950s, the region is the hottest and driest in the United States and the hottest it has ever been in 600 years. Such heat has critically shortened the Scaphiopus couchii toad's larval stage. So, desert toads were unable to react in new ways to experimental pond water level changes as they already had the shortest larval period they can tolerate.

While many of a given species will die if introduced to a profound change in their environment, Buchholz argues the more hearty and healthy of the species will evolve to survive in a new environment through natural selection. His interest in the desert species is, "How did that process occur exactly?"

"One of the effects from rapid larval development in the desert toads is they don't have certain physical characteristics that their cousins in wetter environments have," explains Buchholz."For example, the desert spadefoot is smaller and doesn't have the metatarsal tubercles to dig, and they don't have their gonads differentiated at that point."

But genetic modifications over time have enabled desert species to not only survive but to thrive in this new and previously inhospitable environment.

In the complex cycle of survival, researchers wondered whether genes changed first or did phenotypic plasticity allow for individuals to survive with genes adapted to desert pools?
Researchers believe their evidence is the best at showing how species' differences may be a direct consequence of phenotypic plasticity to changing environment.

"What we have found about a major unappreciated piece of the explanation is that species differences in physical characteristics may be initially caused by environmental sensitive hormone levels controlling development followed by genetic changes that set the physical shape for morphological difference."

If hormones control development and those hormones are responsive to environment, Buchholz says, then environment can transmit signals by way of temperature, food, predators, stress — anything that impacts the animal to turn hormonal signals into an adaptive response.

Similarly, humans can achieve different body sizes and skin conditions depending on their diets, activity, stress and other environmental factors. Thus differences between species can evolve through the changing of their ancestral physical characteristics - explaining how some changes can become fixed through the process of genetic accommodation.
"We think toad ancestors enabled desert survival because their physical characteristics were flexible and they were able to respond to a drying pool by freaking out and having a stress-induced increase in metamorphic rate. This enabled them to shorten their larval periods from months and weeks to just days by switching on corticosterone stress hormones that act synergistically with thyroid hormones to accelerate the metamorphosis to speed the development."

Daniel Buchholz PhD, Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio, USA

"Eventually this ability becomes fixed as the desert species consistently encountered short duration ponds. This allowed the tadpoles to use newly developed lungs to escape the drying pond and move safely onto land."

Buchholz also thinks toad species living in permanent or semipermanent ponds can prompt their own metamorphosis by sensing their pond is drying up too quickly.
Thyroid glands are critical in frog development, just as in humans. But, spadefoot toads can also activate their adrenal glands. This produces a stress hormone that accelerates metamorphosis in species with naturally longer larval periods.

Buchholz: "Over time, smaller desert toads that survived natural selection developed rapid metamorphosis — but now lack the ability to change their rate of development back in response to new environmental changes. Questions remain open whether mechanisms detailed in our paper will apply to species dealing with modern climate change."

Phenotypic differences among species may evolve through genetic accommodation, but mechanisms accounting for this process are poorly understood. Here we compare hormonal variation underlying differences in the timing of metamorphosis among three spadefoot toads with different larval periods and responsiveness to pond drying. We find that, in response to pond drying, Pelobates cultripes and Spea multiplicata accelerate metamorphosis, increase standard metabolic rate (SMR), and elevate whole-body content of thyroid hormone (the primary morphogen controlling metamorphosis) and corticosterone (a stress hormone acting synergistically with thyroid hormone to accelerate metamorphosis). In contrast, Scaphiopus couchii has the shortest larval period, highest whole-body thyroid hormone and corticosterone content, and highest SMR, and these trait values are least affected by pond drying among the three species. Our findings support that the atypically rapid and canalized development of S. couchii evolved by genetic accommodation of endocrine pathways controlling metamorphosis, showing how phenotypic plasticity within species may evolve into trait variation among species.

Authors: Saurabh S. Kulkarni, Robert J. Denver, Ivan Gomez-Mestre, Daniel R. Buchholz

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Oct 27, 2017   Fetal Timeline   Maternal Timeline   News   News Archive

Three spadefoot toad species at the same stage, beginning metamorphosis, but at different ages.
Top: 20-day-old Pelobates cultripes; Middle: 13-day-old Spea multiplicata;
Bottom: 7-day-old Scaphiopus couchii (desert). Image credit: University of Cincinnati.

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