Allonursing – what are the benefits?

I wrote a while back to ask – is “cooperation” really cooperation if it imposes no cost on the giver? Two things are usually assumed about cooperative behaviours: that they incur a cost to the participating individual, and that they provide a benefit to the receiver. Back then I’d recently shown that subordinate female meerkats that allonursed (provided milk to offspring that weren’t their own) didn’t, as expected, lose a significant amount of weight while doing so relative to other subordinate female helpers in the group, suggesting that the long term costs of allonursing weren’t high at all – the opposite of what I’d expected to find!

But what about the benefits of this behaviour?  This is what I tried to find out next in an analysis that has recently been published in the Journal of Animal Ecology. For allonursing to really be a cooperative behaviour in meerkats, it should provide benefits to the individuals actually receiving the extra milk (pups), and possibly also their mothers, who might be able to reduce their own input because their babies are getting food from another source.

As a reminder, in meerkats, only one dominant female breeds while other females help her to rear her offspring without necessarily having any of their own. In this system, unlike in communally breeding species where females all nurse each others’ young, the costs and benefits should be easier to figure out because only one “type” of female provides milk (subordinate aloneness) and one “type” of female receives the benefits (dominant females whose pups are allonursed)…

… like this!

Capture
In communally breeding species (a) mothers are simultaneously donors and recipients of allonursing, meaning that while mothers and offspring may benefit from offspring receiving allonursing, quantification of these benefits is likely to be confounded by costs (energetic costs to mothers of providing milk to non-offspring, costs to offspring of maternal resources being diverted to non-siblings). In singular cooperative breeders (b) only one female in the social group produces offspring, which are raised by subordinate helpers (denoted “SUB”) not concurrently rearing young of their own, so help is not reciprocal. Resultantly, the costs of providing allonursing are not confounded by the benefits of receiving it and vice versa. Dashed lines enclose individuals likely to incur costs through allonursing; dotted lines enclose individuals likely to benefit from allonursing. Small circles denote offspring.

So what benefits might we expect to see pups and mothers gain from the lactational attentions of a subordinate female?

PUPS: For baby meerkats, and many other mammals, milk is the primary source of nutrition in early life, and so we’d expect that (as for all of us – sigh) getting more nutrition would mean gaining more mass (Koenig 1997). And gaining mass at this stage of a mini-kat’s life is good news, as heavier pups are more likely to survive to grow up as potentially reproducing adults in the social group (Russell et al. 2002)…

© 2007 Ron Reznick www,digital-images.net [#Beginning of Shooting Data Section] Nikon D2X Focal Length: 200mm Optimize Image:  Color Mode: Mode II (Adobe RGB) Long Exposure NR: Off High ISO NR: Off 2007/08/20 11:03:57.2 Exposure Mode: Aperture Priority White Balance: Color Temp. (5300 K)  Tone Comp.: Less Contrast RAW (12-bit) Metering Mode: Multi-Pattern AF Mode: AF-C Hue Adjustment: 0° Image Size: Large (4288 x 2848) 1/350 sec - F/4 Flash Sync Mode: Not Attached Saturation: Normal Color Exposure Comp.: 0 EV Sharpening: Normal Lens: VR 200mm F/2 G Sensitivity: ISO 200 Image Comment: (c)RonReznick_www.digital-images.net [#End of Shooting Data Section]
For meerkat babies, chunky is funky © 2007 Ron Reznick
http://www.digital-images.net

MOTHERS: For meerkat mothers, the benefits are perhaps a little less clear. They don’t actually receive any food themselves – but, it’s possible that by their offspring receiving food from another individual, it frees up their time to forage more and nurse less, or reduces the energetic demands on them in terms of milk production. If this was the case, we’d expect that mothers with allonursing help should be in better condition when the pups are ready to forage for themselves than mothers who have to carry the burden of lactation alone. Being in better condition also has implications for other aspects of maternal life – such as reducing the time to the next pregnancy.

To try and figure out how allonursing influences measures of pup condition, and maternal condition, and how these things might all be interlinked (along with environmental and social factors in a great web of ecological complexity), I constructed (with the help of the wonderful Katie McGhee) a structural equation model.

Simplified structural equation model, arrows depicting expected relationships
Simplified structural equation model, arrows depicting expected relationships

Above is a simplified version of what we created – which was basically a web of relationships, which we specified based on knowledge of the meerkat system (in other words, we know that rainfall = heavier mums = larger litters, so we could specify those “paths” in the model). We then specified paths between allonursing and the things we expected it to influence, and tested the fit of the full model – and hooray, it fit the data! Then, to determine how important allonursing is in these patterns, we took it and its paths out of the model, and re-tested the fit, with the predictions that if it’s important in the patterns specified in the model, a model without allonursing in it should not fit the data. But – surprise! – the model without allonursing fit the data just fine — telling us that the influence that allonursing has on pup mass (g), survival, and maternal condition and lactation duration were not important.

[I really would recommend this model structure. With messy ecological data — and honestly, isn’t that everyone-who-doesn’t-work-on-experimental-systems data? — this really gives you a sensible framework within which to test predictions not just about linear relationships between two variables, but how a variable influences multiple patterns. This paper was a must-read for me – and there’s a whole book available online about the use of SEM in natural systems. Have a look! I’m happy to answer basic questions about how/why to use it.]

But back to the meerkats – and the strange lack of benefit that allonursing appears to provide (or not!). There are a couple of explanations for why we didn’t find the obvious benefits of allonursing that we were expecting to.

  • we were looking at the wrong things – for example, Roulin & Heeb (1999) suggest that pups might benefit from nursing from a number of females as it might allow them to get different types of immune compounds in the milk they receive from multiple sources, resulting in a stronger immune profile that might have a better chance of fighting off diseases. Unfortunately we haven’t yet found a way of sampling milk from the meerkats so haven’t been able to test whether different females differ in what immune compounds are present in their milk.
  • the evolution of allonursing might not be driven by the benefits to recipients, but because the costs are low for the allonurses themselves (MacLeod & Lukas 2014). If you don’t have much money, a fiver seems like a lot, right? But, when you have £100 and it’s going to disappear in a few days, giving away a fiver doesn’t seem like that big a deal. That could be the scenario that subordinate female meerkats find themselves in, especially if they have recently given birth or lost pups to infanticide, and have excess milk… Being charitable with their resources also might benefit them in the long run via…
  • social benefits to allonurses. Were we looking for benefits in the wrong place? It’s possible that subordinate females allonurse more to curry favour with the dominant female than to actually provide milk to hungry pups – a clever move, especially if sucking up to the dominant female means you’re less likely to receive aggression or be chucked out of the group (this is something I’m moving on to look at in the future!)

What we really need to figure out, in order to answer these questions, is how much milk subordinate females are actually passing on to offspring when they allonurse. As I mentioned, we haven’t yet found a way of measuring this in wild meerkats – a project for the future!

References:

Koenig, B. (1997) Cooperative care of young in mammals. Naturwissenschaften, 84, 95–104.

MacLeod, K.J. & Lukas, D. (2014) Revisiting non-offspring nursing: allonursing evolves when the costs are low. Biology Letters, 10, 20140378.

Roulin, A. & Heeb, P. (1999) The immunological function of allosuckling. Ecology Letters, 2, 319–324.

Russell, A.F., Clutton-Brock, T.H., Brotherton, P.N.M., Sharpe, L.L., Mcilrath, G.M.F., Dalerum, D. et al. (2002) Factors affecting pup growth and survival in co-operatively breeding meerkats Suricata suricatta. Journal of Animal Ecology, 71, 700–709.

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One thought on “Allonursing – what are the benefits?

  1. Pingback: New Year’s Resolutions | Dr Kirsty MacLeod

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