Abstract

Baby zebra finches hatch into one of Earth's most inhospitable environments, the Australian outback, where summer temperatures can exceed 40°C. Fortunately, zebra finch parents can prepare their young for this dangerously hot climate by singing to them before they hatch. When temperatures rise above 26°C, parents emit ‘heat calls’ that warn their embryos of high environmental temperatures. Unlike their normal vocalizations, heat calls have a high-pitched frequency, a fast rhythm and can prompt embryos to develop differently in preparation for the heat. Notably, birds that are serenaded by heat calls as embryos tend to be relatively small, a characteristic thought to help them lose heat more efficiently and produce more young throughout adulthood. Despite the lasting influence of heat calls on zebra finch physiology, the mechanism through which they act remains a mystery.Led by Eve Udino (Deakin University, Australia), a team of researchers also from Deakin University, Clemson University, USA, and the Doñana Biological Station, Spain, questioned whether the energy-generating units inside cells (mitochondria) are the missing piece to this musical puzzle. Mitochondria use oxygen to convert food into cellular energy (ATP), while a portion of this oxygen is also diverted to produce heat. Since changes in mitochondrial function during development can have long-term effects on animal physiology, Udino and colleagues suggested that zebra finch mitochondria may be responding to heat calls produced by their parents. The team collected eggs from zebra finches maintained at an outdoor aviary in Geelong, Australia, and incubated the eggs at a blistering 37.5°C. A few days before they were due to hatch, the team played recordings of heat calls to the developing embryos. The newly hatched chicks were then raised in nests at various temperatures, ranging from 22°C to 34°C. Once they turned 13 days old, the team obtained some blood from the chicks to assess the function of the mitochondria in their red blood cells.The researchers first discovered that nest temperature can alter how well zebra finch mitochondria work. The birds raised in hotter nests had less efficient mitochondria, meaning that their mitochondria produced less ATP and consequently more heat than the mitochondria of birds raised at cooler temperatures. Remarkably, embryonic exposure to heat calls improved mitochondrial efficiency across all nest temperatures (22–34°C), suggesting that heat calls re-program how zebra finch mitochondria balance ATP versus heat production.While a nest temperature of 34°C may seem hot, zebra finches can experience temperatures that are much, much higher. Therefore, Udina and colleagues took the study one step further and exposed a group of the 13-day-old birds to a brief heatwave, warming the youngsters’ nests to 44°C over the course of 2.5 hours before checking the mitochondria again. This time, the mitochondria of birds that had listened to heat calls as embryos tended to be less efficient. Although this may seem disadvantageous, the team suspects that there may be benefits to reducing mitochondrial efficiency under extreme heat conditions. High rates of mitochondrial ATP production can produce toxic reactive oxygen species, compounds that can wreak havoc on proteins, lipids and DNA. Making mitochondria less efficient at extremely high temperatures may help birds reduce the damaging effects of reactive oxygen species.We often think that a bird's life begins once it hatches, but birds can sense and respond to events going on in the outside world before they enter it. As zebra finch parents sound the heat alarm, their embryos get to work altering their physiology. So, next time you hear zebra finches calling in the Australian heat, don't think of their sweet songs as ‘music to the ears’, but rather, as ‘music to the mitochondria’.

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