From mothers to eggs – maternal anti-influenza antibody transfer in Mallards

A Mallard nest. Photo by Flickr user nottsexminer, used under a CC BY-SA 2.0 license.

A Mallard nest. Photo by Flickr user nottsexminer, used under a CC BY-SA 2.0 license.

By Jonas Waldenström

I have spent the last two days at home nursing one of my offspring that has been down with a cold. Actually, since this is the oldest daughter, nursing generally involves providing her with unlimited access to her mother’s iPad and all the sandwiches she cares to eat.

The added benefit is that I have had more time to read and think than I usually have, far away from the office turmoil. So while I have time, I thought I could toss in yet another blog post.

A few months ago I served as an external examiner on Jacintha van Dijk’s PhD thesis in the Netherlands. That was an enjoyable experience – because of the quality of the thesis, and the unfamiliar and ancient procedures of a Dutch defense. I got to wear a funny hat and toga, there was a whole lot of ceremonial ‘all rise’, some marching in and out of rooms in predetermined processions, and other strange things that we don’t do in Sweden.

Anyway, most of Dr van Dijk’s papers are now published, and today I reread a story on maternal antibodies against avian influenza virus in Mallards, published in PLOS ONE this November.

For animals, the energy put into rearing offspring is a substantial investment. Generally, the more you invest the better chances the offspring has to reach reproductive age. However, as all things in ecology, energy isn’t endless, and animal needs to trade-off investments in one life history parameter to those of other parameters. For instance, in animals with several breeding seasons, current reproduction needs to be balanced with survival.

The last 15 years, ornithologists have looked into allocations of maternal antibodies between mothers and offspring. When an egg is laid some of the antibodies of the mother can pass over to the yolk, providing the hatching chick a kick-start of antibodies to fight infections. Such maternal antibodies do not last more than a few weeks, but may nevertheless be important in the early stage of a chick’s life. For instance, this is seen in commercially reared chickens, where maternal antibodies against Campylobacter can protect the chicks from colonization up to two weeks. It has been argued that the mother can choose how much antibodies different eggs receive, thereby modifying the future prospects of her offspring.

In this paper, the Dutch team investigated deposition of anti-influenza antibodies in Mallard eggs. They collected eggs from free-living Mallard nests – which is quite an achievement, since the nests are often tucked away and camouflaged. They also investigated eggs from captive ducks, more conveniently situated in a pen just outside the research institute.

Antibody concentrations were determined in both egg yolk and in the blood of the mothers, and they controlled for egg size, embryo sex, egg laying order, and female body condition. However, first they needed to check whether the incubating female indeed was mother to all the eggs in the clutch, since mallards are notorious egg dumpers.

Association between the AIV antibody concentration in egg yolk and female serum from (A) the field study and (B) the captive study. Note: axes are minuslog10-scaled. (From the original publication doi:10.1371/journal.pone.0112595.g001)

Association between the AIV antibody concentration in egg yolk and female serum from (A) the field study and (B) the captive study. Note: axes are minuslog10-scaled.
(From the original publication doi:10.1371/journal.pone.0112595.g001)

Indeed, maternal anti-influenza antibodies were found in Mallard eggs from antibody positive females, similar to earlier studies conducted on gulls. There was a positive correlation between antibody concentrations in the eggs and the concentration in the females, but there was no effect of any of the other investigated factors, including the body condition of the female. One more thing, though: there seemed to be an increasing concentration of antibodies with egg laying order; thus, later laid eggs had higher concentrations of antibodies than the early eggs in the clutch.

It remains to show whether this maternal transfer confers protection against influenza virus infections in young mallards, but it is an interesting finding. If maternal antibodies do protect, that could potentially affect local perpetuation patterns of flu, by temporarily reducing the general number of susceptible animals. Or if the antibodies are specific to only those subtypes that infected the mother (which is likely), it could potentially affect subtype distributions in the population, favoring subtypes that are antigenically different. However, if maternal antibodies wane after a few weeks, these effects, if any, should be transient.

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A German Teal and some epidemiological hand waiving

A teal - stunning little bird. But also at present in the center of H5N8 flu business. (Picture from http://www.rspb.org.uk/).

A teal – what a stunning little bird! But also at present in the center of H5N8 flu business. (Picture from http://www.rspb.org.uk/).

By Jonas Waldenström

As most of you know by now, we have a new highly pathogenic avian flu virus in our midst. This virus, of the H5N8 subtype, has been detected in Germany, the Netherlands and the UK in the last two weeks.

The epidemiology of highly pathogenic viruses is quite different from that of their low pathogenic cousins. While low pathogenic viruses are essentially waterfowl viruses, and generally benign, highly pathogenic viruses tend to mainly go rampage in domestic poultry, and are not disseminated broadly in wild bird populations. One important exception is/was the H5N1 virus, that apart from affecting the poultry industry also caused several outbreaks among wild birds in Europe in 2005-2006, but with varying pathogenicity in different avian species.

The new H5N8 virus entered the European scene quite unexpectedly. The closest described outbreak before Germany was Southeast Asia, where this virus had been detected in poultry (and some wild birds) in Korea, China and Japan. That’s quite a leap for a microbe, nearly halfway around the globe.

Phylogenetic studies have confirmed that the current outbreak strain is genetically highly similar to the virus from Asia. Thus the question is really: how the heck did it get here? Officials from OIE and others were quick to point the gun at wild birds. But regardless of how well we know that waterfowl can be hosts of low pathogenic viruses, and that some species can harbor highly pathogenic viruses asymptomatically, there are no direct migration routes in autumn between the two areas. Thus, if the virus entered Europe via wild waterfowl it must either been around in wild bird populations for a longer time, allowing sequential transmission between different populations/species at shared breeding or stopover sites, or there might have been undetected outbreaks in poultry further west (e.g. Russia) where virus has disseminated into wild bird populations migrating westward. Neither do we know how this particular virus affects wild birds – is pathogenic to waterfowl, does it interfere with migration, how long do infected birds shed virus, etc?

An alternative hypothesis, of course, is that it has reached Europe as part of the trade with poultry and products. After all, the chicken is the most common migratory bird on the planet, although it doesn’t fly on its own wings.

The ‘chicken vs. duck’ argument is an inflamed old discussion, where different people tend to have polarized positions. In my opinion, a middle stance is more appropriate. Likely, both wild birds and poultry can affect geographic spread of highly pathogenic viruses, but the circumstances may act differently from case to case.

The biggest problem at present is our lack of data. A few days ago, the H5N8 virus was identified in a Teal shot as part of active surveillance in Germany. Depending on your preferences, this finding in a healthy duck (that’s at least what the reports say) could either be a ‘game changer’, providing evidence for a link to wild birds, or a spillover event from poultry to wild birds.

Instead of arguing based on a single Teal, we need to gather much more data. And do so quickly. We should ramp up active surveillance in both poultry and wild birds. During the H5N1 years, a network of ornithologists and virologists was created that substantially contributed to the increased knowledge base on influenza A virus epidemiology and ecology. This network was mostly dismantled when the H5N1 virus disappeared from the European scene, but the core is still there and would be easy to gear up again.

Let’s do that, shall we?

————UPDATED————–

As pointed out to me on Twitter and here on the blog, there are indeed more wild bird sequences of H5N8 that are interesting (see here for instance) in this context. This is an interesting virus, and more info is likely to follow. Near identical sequences in wild ducks in Chiba, Japan, to the viruses detected at same time in Germany is indeed a strong argument for wild bird involvement in geographical spread.

However, my main points – that our different preconceptions tend to make the discussion too black and white, and that we need to obtain more data – are still very much valid.

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From Worms Head to The Eagle – and some gizzards too

By Jonas Waldenström

Contrary to many people’s belief, science is actually a very social thing. Ideas are boiled downed to testable hypotheses, many sets of hands help out in the field, catching stuff, measuring stuff, or aid in the lab with fine-tuned molecular wizardry. In the writing phase, coauthors tap away on their keyboards, shuffling paragraphs around, correct grammar (or obnoxiously defend their own pet sentences), before the final manuscript is perused by one or several editors and (somewhat) helpful reviewers. More than that, we meet at work, at conferences, or chat via Skype. It’s all a part of our trade, a connected and mostly friendly social network.

Last week I sailed away on a particularly nice jolly. Having been invited two give talks at two British universities (thanks Ben Sheldon, and Oskar Brattström!). I packed my hand luggage with underwear, shirts and snus to last me a week, and step on to the plane to Heathrow.

My tour took me first to Oxford and the Edward Grey Institute, then down to Swansea for Campylobacter discussions and some French cuisine (and when I say French, I mean the proper sense: confit de canard and a poultry gizzard salad), and then over to the Zoology Department in Cambridge. This sort of travel is really fantastic. Apart from giving my talks, I also had the opportunity to chat with a range of different scientist. I listened to a number of genomics talks in Oxford, got to see a specimen of the Hoff crab, discussed fear in badgers over a few pints at The Turf, had more beer at The Eagle in Cambridge (where Crick exclaimed to the world that he and Watson had ‘discovered the secret of life’), and had great discussions with colleagues on antigenic structures in influenza viruses, migration of ducks in Georgia, and of gene flow between Campylobacter in wild birds and domestic animals. In all, a smorgasbord of thought.

Of course this left me a bit drained, and it was good to get home to the family again. But wow, being an academic has its upsides!

Rinse the gizzards, fry them in duck fat, serve with salad, blue cheese and walnuts.

Rinse the gizzards, fry them in duck fat, serve with salad, blue cheese and walnuts.

The dramatic coastline at Worms head, Swansea

The dramatic coastline at Worms head, Swansea

The Turf - just a short walk from the Zoology Department in Oxford

The Turf – just a short walk from the Zoology Department in Oxford

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Happy grant feet

By Jonas Waldenström

A few days ago I wrote about the pain of the grant decision limbo. Similar to traditional torture, the whole process is honed to perfection to maximize researchers’ pain. This Friday, at long last, the decision I had waited for was scheduled to be announced. The whole day I checked the homepage again and again. First every hour, and then every 10 minutes or so. And suddenly, after the 100th time I had clicked the link, the decision was out.

Some moments stretch out for ever. The computer did the rolling green snake, working its way through a busy server while downloading the list.

The feeling of finding your name on the list of funded projects is incredible. First a great relief, followed by tremendous joy. On your toes, happy feet, bounce, shout, and then back to check that your project was really listed there. And fuck, it is there, it really is! And that’s when the true recognition hits you: I bloody nailed it! I can do the science I want to do. I can hire. I can do sweet, sweet science, long time!

Thus, time to rejoice. Plan with coworker, get the project going.

Next spring it is time again, a new round of application writing. This time for continued funding of influenza research. But for now it is good, all good.

 

An awful week in the Ivory Tower

Photo by Flickr user Paul Simpson used under a CC BY-ND 2.0 license

Photo by Flickr user Paul Simpson used under a CC BY-ND 2.0 license

By Jonas Waldenström

This is an awful week to work in the Ivory Tower. Outside the office window the November rain forms puddles on the tarmac. It is dark, and with each passing day the sun climbs even lower on the horizon and the nights become longer. This dark and wet week is also when the Swedish research councils VR and FORMAS decide who is going to get funded in the next coming years.

The announced day is a dreadful day for all whom have long waited to hear back on their applications. Will it be funded or turned down? Who got, and who did not? The problem, of course, it not so much the fact that we compete for funding, but that so few can be awarded. Most do not pass the cut. In fact, this Monday when VR posted their list, 333 of 2700 projects were funded in natural sciences. That’s a staggering 84% of very disappointed grant-writing researchers. And a happy 16%…

It is a long process: applications were submitted in April, then perused by different advisory boards over summer and autumn, before finally the sums are set and the decisions become public.

This year my hope lies with FORMAS, where I have submitted a proposal on Campylobacter ecology and evolution based on full genome sequencing and infection experiments. It is a nice application, with great collaborators, and I have a good track record in the field. But it is nerve-racking nonetheless. The cut at FORMAS is roughly the same as for VR (though both seems to fund slightly more proposals than last year), so it will be a though call. When the decision is taken, the cut cross ruthlessly through a heap of very good proposals.

I will know on Friday. Until then: the pain.

Finally, a suggestion: dear funding agency, couldn’t we flip the academic fiscal year so that we apply in November and get the results in spring? That way even a grim decision can be carried, the loss lessened by the arrival of songbirds and flowering trees. Please.

(I realize I have covered this topic before; I guess it is some sort of therapy)