I had one of those “I never knew that,” moments reading a paper in Science magazine this week, but, given that the research in question managed to get published in one of the top journals in the field, neither did lots of other people. The “that” in question? That sounds can alter the development of a embryonic bird to enable it to adapt to the environment it can expect when it hatches.

Many species can hear and learn sounds as embryos, and it’s common in birds, for whom song is a major form of communication: in many bird species parents call to their eggs during incubation, and bird embryos at later stages of development can hear and sometimes even make sounds. This serves a variety of purposes: synchronising hatching, improving brain development and learning (I imagine in a way that is similar to a fetus practicing movements in utero), and allowing the embryo and later nestling to solicit attention from the parents.

This relates, a little indirectly, to the science of epigenetics, which has been a hot topic of interest for a number of years. This is probably because for some time the accepted wisdom (and, to be fair, all the available evidence) suggested that the action of the genes you possessed was fairly rigid and couldn’t be altered by environmental conditions. Genomes evolved by mutation: only when genes were copied during the process of making gametes (sperm and egg cells) could accidental mutations creep in that could be inherited by any offspring. Natural selection acted upon these mutations, but also mostly by the simple pack-of-cards genetic shuffling that goes on in a sexually reproducing population, in that the offspring inherit a mix of different versions of genes from the parents (e.g. the blue version of an eye colour gene from one parent, and the brown version from another). The important thing is that selection acts upon the variation that already exists in a population: i.e. how well an organism’s genes predisposed it to be adapted to the environment it found itself in*. Any suggestion that the environment could alter the existing genome of an organism was seen as a throwback to Lamarkism, a pre-Darwinian notion of inheritance that held (incorrectly) that an organism could pass on characteristics acquired during its lifetime to its offspring: in other words, if you developed strong muscles through working as a blacksmith, that your children would inherit strong muscles.

Epigenetics, however, shows that this isn’t the whole story. There’s an awful lot of nonsense and over-hyping around the subject, but essentially what you’re talking about are changes to the genome that aren’t actually changing the DNA sequence that codes for genes, but just what you do with it; specifically, environmentally induced chemical changes that change which genes are turned on and off, what part of the body they are active in, what life stage they are active in, or how much they are turned on (i.e. how much protein product they make). In some cases these changes are heritable, in others they are not; in some they may be transiently inherited by the offspring, but absent in the generation after that. This is largely dependent on the chemical nature of the change performed. There’s no concrete definition of the term, in fact, and some changes that are referred to as epigenetic are not actually heritable, so it’s a bit of a fuzzy area.

The other thing to note is that “environment” in this case is fairly all-encompassing term which includes the environment a developing fetus experiences in the mother’s body: indeed, in mammals, this may be one of the most important contexts. It’s hard to tease out cause-and-effect though; often all you see are correlations, and it’s difficult to pick out the underlying change to the genome. The area that’s received a lot of attention is nutrition, due to the burgeoning obesity crisis in developed nations, and the obvious link between maternal nutrition and the health of their offspring. Perhaps the most compelling is the study of children of mothers who suffered severely restricted calorie intake during the Dutch hongerwinter of 1944-45: these people had an increased risk of obesity and cardiovascular disease as adults. It’s been suggested that the uterine environment “primed” their bodies to expect scarce nutrition after birth and to be efficient at conserving energy; in fact, after the war, food was far more plentiful and they were, in essence, maladapted. Interestingly, children born to mothers who suffered from famine during the Seige of Leningrad didn’t show this increased disease risk – but then, their environment was still nutrient-poor. (Reviewed here; this is full-text open access).

Where does this leave our birds? It’s hard to imagine how sound could alter how the embryo actually develops, or indeed, how a bird can really affect later development at all: after all, once an egg is laid, it’s completely external to the mother’s body, unlike a mammal in which it remains internal until birth. Difficult, you would think, but not, it would seem, impossible. This study demonstrated rather neatly that embryos incubated in higher temperatures than usual were adapted to expect above-average temperatures by the type of calls their parents made to them when they were still in the egg.

zebrafinch
Australian zebra finches: By Keith Gerstung from McHenry, IL, US – Niagara Falls Aviary. https://commons.wikimedia.org/w/index.php?curid=12814136

The researchers originally observed that Australian zebra finches, which live in an arid environment that has a lot of temperature fluctuations, produced an “incubation call” whilst with their eggs: this occurred consistently towards the end of hatching, but only in response to higher temperatures. So they artificially incubated eggs at normal or raised temperatures, playing them recordings of the incubation call or just the ordinary contact calls the parents made, before returning them to nest boxes with naturally different temperatures. This is what happened:

Nestlings exposed to incubation calls as embryos followed a different growth pattern in response to nest temperature than did control nestlings: Treatment nestling mass…on day 13 decreased with nest temperature, whereas it increased in control nestlings…This effect at the end of the nestling period (day 13) was already arising just 1 day after hatching and was observed throughout nestling development.

How does singing affect nestling growth? The study doesn’t get down to the molecular details, but it’s likely to be due to somehow altering hormone-mediated behaviour:

In birds, maternal effects on nestling growth induced by differential hormone concentrations in the egg are partly mediated posthatching by their effects on nestling begging [i.e. soliciting attention from the adults]. Therefore, we investigated whether differences in nestling begging could underlie the differential growth patterns followed by experimental nestlings in response to nest temperatures. Accordingly, in the first 3 days after hatching, treatment nestlings (i.e., incubation call playback) were more likely to call while begging when they had experienced high temperatures in the nest since hatching, whereas control nestlings called less, independently of temperature. Nestling mass and satiation [whether they were hungry or not] at the time of recording had no effect on the probability of calling while begging which suggests that this call might signal thermal state rather than hunger level or body condition.

So the hotter the temperature, the smaller the nestlings, because the calls that their parents had made to them whilst they were embryos had altered their behaviour post-hatching so that their calls were not necessarily food-related. Fascinating – but why would this be advantageous? The authors note that this trend towards decreased size at higher temperatures is consistent with the current pattern observed in many wild bird species worldwide. Possibly this is because a smaller body enables greater heat loss. Whatever the reason, it clearly is adaptive, because further experiments showed that smaller nestlings raised at higher temperatures had greater reproductive success as adults than larger nestlings, with the opposite being true for those raised at cooler temperatures. Of course, as noted for those studies on maternal nutrition and obesity, the environment the nestlings grow into may change unpredictably, but they may well be able to compensate to a certain degree by finding favourable micro-habitats: in fact, during the study, those raised in warmer temperatures consistently then chose warmer nest boxes in which to breed themselves. On a longer time scale, mechanisms such as these may help species adapt to climate change.

*(As an aside: yes, mutations happen all the time in non-gamete cells; usually they don’t do much and are often detected and repaired, or the faulty cell destroyed, but they are the root cause of cancers. However, if you have a random mutation that spontaneously arises in a liver cell, that’s where it’s staying. It might pass to any daughter liver cells, if that cell divides, but it’s not going into your sperm/eggs to be inherited by your children.)

References

Mariette, M. & Buchanan, K. “Prenatal acoustic communication programs offspring for high posthatching temperatures in a songbird”, Science Vol. 353, Issue 6301, pp. 812-814

Schulz, L. “The Dutch Hunger Winter and the Developmental Origins of Health and Disease.” PNAS Vol. 107 No. 39, pp. 16757-16758

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