Category: natural selection

The peppered moth – a video

April 7, 2017 • 8:26 am

by Matthew Cobb

The peppered moth story is one of the best examples of evolution in action. In this brief video, my final year student Tom Parry, tells the whole story, from 19th to 21st centuries. It includes interviews with my colleague Professor Laurence Cook, who carried out some of the recent research confirming how selection acts on the moth, and with Professor Ilik Saccheri of Liverpool University, who has identified the underlying genetic cause of this iconic change due to natural selection. PCC(E) makes a brief photographic appearance, due to the “notoriety” (his term) he attracted in 1998 because of this review.

As with Izzy Taylor’s video earlier this week, Tom needs your feedback – our students have to write a ‘reflective’ piece in which they discuss comments about their videos. So any comments you can make, either below or on YouTube would be gratefully received. If you are a teacher and want to use this with your students, feel free, but please try and collect some feedback from them.

 

A new paper showing the usefulness of the kin-selection model

February 4, 2016 • 9:45 am

There’s a new paper in the Proceedings of the National Academy of Sciences USA by David A. Galbraith et al. (free link and reference at bottom) that has a very cool result: one predicted by kin-selection theory. Kin selection, as you may know, is the idea that the adaptive value of a gene (and hence its evolutionary fate) must include information about how that gene affects its copies in relatives (e.g., a gene in parents for taking care of offspring can promote the replication of the copies that also occur in those offspring). Wikipedia describes this idea pretty succinctly.

Kin selection has been a very useful concept in understanding things like behaviors directed at offspring and relatives, and particularly in understanding the evolution of altruism and of one of its forms: eusociality—the behavior in which a colony of individuals is divided up into castes, some of which reproduce and some of which are nonreproductive but tend the “queen’s” brood (honeybees and naked mole rats are examples).

There are a few people, though, most notably Martin Nowak and E. O. Wilson at Harvard, who have questioned the usefulness of kin selection, arguing that group selection theory (or “multilevel” selection theory) is the only way to study the evolution of eusociality. I’ve written a lot on this site questioning their ideas (see some links below) as well as their claim that kin selection is not a useful way to study evolution in nature. The paper below, I think, shows the usefulness of the kin-selection paradigm, which seems to make predictions—ones that are verified—that don’t flow in any obvious way from a perspective of group or multilevel selection.

Because the paper is complex, I’ve asked my friend Phil Ward, a professor of entomology at the University of California at Davis (and a student of insect evolution) to explain its predictions and results. His explanation may be a bit difficult for non-biologists, but there is no simpler way to explain the study. Give it a go!

 

by Phil Ward

There has been a vociferous debate over the relative merits of group selection theory and inclusive fitness theory (or kin selection theory) as explanations for the evolution of altruistic behavior, especially following a contentious paper by Nowak et al. (2010) which claimed the superiority of the group selection approach. This was met with a resounding rebuff by a large group of evolutionary biologists who argued for the much greater explanatory power and heuristic value of inclusive-fitness thinking (e.g., Abbot et al. 2011). Some previous postings on WEIT about this topic have appeared here, here, here and here.

One fruitful area of inquiry in which kin selection theory makes explicit and testable predictions is in the study of genomic imprinting, a form of intragenomic conflict in which there is differential expression of genes inherited from the mother versus the father. In a theory paper published more than a decade ago, David Queller pointed out that this form of intragenomic conflict can be expected to be particularly widespread in colonies of social insects, and he employed kinship theory to predict the outcome of such conflict under different social contexts.

Now a recent empirical paper by Galbraith et al. (2016) provides convincing evidence that intragenomic conflict in honey bees indeed reveals itself in a way predicted by kin selection theory.

The authors first point out that genes inherited from mothers (matrigenes) and those inherited from fathers (patrigenes) are expected to be in conflict in honey bee workers that have an opportunity to reproduce. Why? Because a honey bee queen mates with multiple males, and the resulting workers are mostly half-siblings. These half-sibling individuals share half of their matrigenes but none of their patrigenes (see Figure 1 of the paper). So, consider a colony in which the queen has died, and half-sibling workers begin to compete over egg-laying (this behavior is inhibited by the queen while she is still alive). A worker’s matrigenes can be passed on when either she or her siblings reproduce, but her patrigenes are present only in her own offspring. Hence, as the authors put it, “compared with matrigenes, patrigenes will favor worker reproduction and exhibit enhanced activity on worker reproductive traits”.

This prediction was tested by quantifying the extent of genomic imprinting, i.e., the differential expression of genes of paternal origin.

The authors’ predictions were upheld. Using a series of genetic crosses that allowed them to distinguish matrigenes from patrigenes, they found that workers in queenless honey bee colonies showed greater expression of paternal than maternal genes, and this patrigene-biased expression was even higher in those workers that actually reproduced. In addition, when comparing parent-of-origin effects on reproductive traits such as ovary size and ovarian activity, patrigenes were shown to exert a much greater influence than matrigenes.

It should be emphasized that the worker reproduction occurring in queenless honey bee colonies produces only one sex: males.The workers lay unfertilized eggs and, as a consequence of the peculiar genetic system (haplodiploidy) found in bees, wasp and ants, these haploid eggs develop into males (which thus carry only one set of chromosomes). With no further production of workers, the colony will soon decline.

So, this last gasp of haploid reproductive effort that occurs when a queen dies (and is not replaced) will have selective significance only if the males that are produced have an opportunity to mate with queens from other colonies, something that takes place in population-wide mating swarms. Presumably this process of rearing and releasing drones (male bees) in a timely manner works best if some workers reproduce while the remainder continue to forage for food and feed the developing drone brood. Thus, colonies in which all reproductively capable workers give in to their patrigenic impulses might produce fewer reproductively successful drones than those in which there is some degree of reproductive restraint by the workers. One could argue that this is a kind of “colony-level” selection that weeds out disruptively high levels of patrigene expression, but inclusive fitness theory would explain this as a consequence of cost-benefit ratios that moderate the expression of both matrigenes and patrigenes.

Finally, for the small fraction of workers in a honey bee colony that are full siblings, the genetic interests of matrigenes and patrigenes are quite different: patrigenes can be equally well propagated through a worker’s own reproduction or that of a full sibling. Most competition for reproduction in honey bees is among half-siblings, however, so this should have little effect in honey bee colonies. Nevertheless, among other social insects in which the queen mates only once (such as bumble bees and many species of ants) all workers are full siblings and, as the authors note, the prediction is reversed: matrigenes should favor worker reproduction and show enhanced gene expression relative to patrigenes. Apparently this has not yet been studied, but it would constitute an elegant complementary test to the ground-breaking results of Galbraith et al.

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Honeybee workers surrounding their queen, who’s been marked with a dot

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Galbraith, D. A., S. D. Kocher, T. Glenn, I. Albert, G. J. Hunt, J. E. Strassmann, D. C. Queller, and C. M. Grozinger. 2016. Testing the kinship theory of intragenomic conflict in honey bees (Apis mellifera). Proc Nat. Acad Sci. USA 113:1020-1025. doi:10.1073/pnas.1516636113

 

 

 

New paper shows that Nowak et al. were wrong: kin selection remains a valuable concept in evolutionary biology

March 27, 2015 • 11:30 am

In 2010 three authors—Martin Nowak, Corina Tarnita, and E. O. Wilson—published a paper in Nature (reference and link below) purporting to explain the evolution of eusociality in insects: the phenomenon whereby a colony contains different “castes” that perform different tasks, and at least one caste is sterile.  In bees, for example, there is usually a single fertile queen, who produces all the offspring, a bunch of sterile working females (“workers”) who defend the nest and tend the brood, and fertile male “drones” who do basically nothing but compete to mate with the next generation of queens. Nonreproductive castes are general (though not ubiquitious) in the Hymenoptera (ants and wasps), as well as in some other animals like termites (Isoptera) and naked mole rats.

It’s hard to understand how it could be advantageous for some individuals to evolve sterility, which, of course, seems patently maladaptive. Darwin was the first to notice this problem. At any rate, one solution involves the notion of kin selection: the idea that a gene can promote sacrificing your own personal reproduction if it more than compensates for that loss by increasing the number of relatives you have—relatives who also carry copies of the “sacrifice” gene. It turns out that under a simple calculus that involves weighing the reprodutive benefit to relatives (discounted by the degree of relatedness) versus the cost of sacrificing your own reproduction, you can indeed evolve genes that cause you to lose reproductive ability—so long as they increase it in your relatives.

Such kin selection was an important explanation for the evolution of eusociality. Some think it’s because of the peculiar “haplodiploid” nature of inheritance in Hymenoptera, whereby the male who fertilizes the queen is haploid (has only a single set of chromosomes), and the fertile queen is diploid, with the normal two sets. In such a case, the female workers are more related to their sisters than to their own offspring, which may help them evolve the tendency to stop having their own offspring and produce more sisters; i.e., become sterile and help the queen raise her brood. Others question the importance of haplodiploidy in eusociality.

But the evidence for kin selection and relatedness is still clear. For example, eusociality in Hymenoptera has evolved several times, but always occurred in an ancestral lineage in which queens mated singly rather than multiply: a statistically significant finding (Hughes 2008; reference and free link below). That’s important because in such cases offspring are more related to each other than offspring produced by different fathers. Further, Bob Trivers showed that other patterns in bees, ants, and wasps—especially the observed ratios of males to reproductive females in colonies—also followed the dictates of what kin selection predicted. There are still other behavioral recognition experiments of kin versus non-kin supporting the importance of relatedness.

Nowak et al.’s paper, however, attacked this body of knowledge, claiming that kin selection and relatedness were not only unimportant in the evolution of eusociality, but were unimportant in general. (Ed Wilson has spent the last five years, for instance, arguing in his books and talks that kin selection is a misguided notion in evolutionary biology, and that group selection is far more important.) Nowak et al. used a rather complicated model of colony selection in which mother and all offspring were genetically identical and argued that relatedness was a consequence of the evolution of eusociality and not a driver of eusociality.

As I noted at the time, their dismissal of relatedness and kin selection from their model seemed bizarre, since they didn’t vary relatedness in their model. If you don’t do that, how can you say it’s unimportant in evolving eusociality? And people in the field found other problems with both Nowak et al.’s model and their conclusions about the uselessness of kin selection (go here for all my many posts on this issue). Over 120 experts in the field, for example, wrote a letter to Nature criticizing the conclusions of Nowak et al. But Nowak, Tarnita, and Wilson have remained obdurate.

Now, a new paper in PLOS Biology by Xiaoyun Liao, Stephen Rong, and David Queller (reference and free link below) shows not only that the model of Nowak et al. was bizarre, with little obvious relationship to the evolution of eusociality, but was also flatly wrong its three major claims about the evolution of eusociality.

What Liao et al. did was simply vary the relatedness and other assumptions of Nowak et al.’s model. After doing that, they found that the original authors’ claims about the generality of their model were incorrect. Keep in mind that Liao et al.’s conclusions were based simply on manipulating the very model that Nowak et al. used to claim the irrelevance of kin selection, or on deriving new equations using Nowak et al.’s exact modeling strategy.

Here is what Liao et al. found, contra Nowak et al.:

1. Relatedness does help the evolution of eusociality, so kin selection is not irrelevant.  Unlike Nowak et al., Liao et al. varied total relatedness by allowing a certain fraction of offspring in the nest to be unrelated to the “queen” rather than simply her clones. (This could occur by immigration of insects from other nests, or by queens laying eggs in other queens’ nests.) What they found is that relatedness indeed makes a big difference: under conditions in which worker behavior is affected by their own genes rather than just the queen’s, eusociality evolves much more easily when relatedness between queen and “worker” is higher. In other words, higher relatedness (kin selection) is causal in this circumstance, not just a consequence of the evolution of eusociality. Nowak et al. were wrong, and all the statements of this group about the uselessness of kin selection based on this model are also wrong.

2. Workers’ evolutionary interests can differ from those of the queen. Nowak et al. saw workers as “evolutionary robots” who could not have an evolutionary strategy differing from that of the queen. This was a bit weird, since we’ve known from experimental and natural history data that there is a conflict between queen and workers (predicted by kin selection theory), and the results of that conflict are seen in the sex ratios produced in nests. Further evidence for that conflict occurs when the queen produces more males than the workers “want” (i.e., more than is in the workers’ genetic interests), and in that case the workers kill those males. This wouldn’t happen if the interests of queens and workers were coincident.

Liao et al. showed that varying how the genes for worker behavior and sterility were expressed—whether in queens alone or in offspring alone—had a substantial effect on the probability of evolving eusociality. As kin-selection theory predicts, eusociality evolves much more easily when the queen has absolute control over the behavior (and fertility) of her workers. When workers get a say—that is, when their own genes rather than just the queen’s genes control their own behavior—it’s not so easy to evolve eusociality, for workers sometimes have an evolutionary impetus to produce their own offspring rather than just raise the queen’s. This shows, as kin selection predicts and observation shows, that there is indeed a conflict between the interests of the queen and the workers.

3. Eusociality isn’t as hard to evolve as Nowak et al. assert.  In their paper Nowak et al. claimed that eusociality is “hard to evolve.” It’s difficult to evaluate this claim because you have to ask, “Hard relative to what?” But Liao et al. showed that some of the difficulty in the Nowak et al. model is because of two wonky assumptions: 1). Below a certainly colony size no worker can add anything to the offspring production of the colony, while 2). above that threshold there is a fixed output of offspring that does not change with the addition of more workers.

This seems completely unrealistic, for why wouldn’t two workers add more offspring than one, and why, over the threshold, wouldn’t more workers help produce more offspring by defending the nest better and tending more brood? Further, why would workers in large colonies remain in those colonies, since their presence adds nothing according to the “threshold” model? They should, instead, join smaller colonies, pushing them over the threshold. And indeed, when Liao et al. added more realistic assumptions to Nowak et al.’s model—a “stepwise” feature whereby, up to some limit, each worker adds an increment to the offspring production of the colony—eusociality evolved more readily.

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So what is the upshot? First, that kin selection, i.e., the relatedness between queen and her offspring, plays an important causal role in the evolution of eusociality.  Nowak et al. were dead wrong in denying this. And since the subsequent statements of both Nowak and Wilson on the evolutionary worthlessness of kin selection were based on a model that could not show what they claimed to show (because relatedness wasn’t allowed to vary), we should not take their dismissal of kin selection seriously. Kin selection remains a viable and valuable view in evolutionary biology—indeed, one of the most important advances since the 1950s—and, as I’ve shown in my earlier posts, has helped us understand a wide variety of biological phenomena.

The other points are less important, but still show that Nowak et al.’s model was too narrow to support their generalizations about no conflict between queens and workers, or about the “difficulty” of evolving eusociality. Yes, it may indeed be hard to evolve such a bizarre system, and it may require uncommon ecological and/or genetic circumstances, but it’s not as hard, at least in theory, as Nowak et al. maintained.

The final lesson is that one’s biological conclusions from a model are only as good as the biological assumptions built into it. Because Nowak et al.’s assumptions were flawed, and because they failed to examine the robustness of the model to varying its assumptions, they arrived at faulty conclusions. But because Nowak and Wilson were already famous evolutionary biologists (particularly Wilson, who is an iconic figure in the field), and because the paper was published in Nature, their conclusions were taken far too seriously. The paper should have been reviewed by more critical reviewers in the field. Even I, who do not work on the evolution of eusociality, could see that you can’t dismiss the value of genetic relatedness from a model in which relatedness isn’t allowed to vary!

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Hughes, W. O. H., B. P. Oldroyd, M. Beekman, and F. L. W. Ratnieks. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213-1216.

Liao, X., Rong, S., and D. Queller, 2015. Relatedness, conflict, and the evolution of eusociality. PLOS Biology | DOI:10.1371/

Nowak, M. A., C. E. Tarnita and E. O. Wilson.  2010.  The evolution of eusociality.  Nature 466: 1057-1062.

 

Guest post: Natural selection in real time via road kill

March 30, 2013 • 6:00 am

by Greg Mayer

A new paper in Current Biology by Charles & Mary Brown with the folksy title, “Where has all the road kill gone?”  reports evidence for rapid evolution of wing length in cliff swallows (Petrochelidon pyrrhonota) nesting on highway overpasses in Nebraska. (See also this news piece on Science‘s website.) For those evolution-deniers who demand to see natural selection in “real time,” this is one bit of evidence.

During the course of a 30-year field study, the Browns found that the number of road killed birds declined, from about 20 per year, to about 4 per year (panel A in the figure). They could rule out most of the obvious possibilities: the bird population size had not declined (panels A & D), and they had not changed their survey effort or methods. They then compared the wing length of the road killed birds to a sample of the population at large (obtained from netting fatalities, but corroborated by released birds), and found that wing length had declined by several millimeters (panel B) and that the change was cumulative over the 30 years, with the road-killed and population at large birds slowly diverging (panel C; I must say I’m a little perplexed that the dead birds keep getting bigger).

A. Roadkill declines, but the population increases. B. Road-kill birds have shorter wings than the population at large. C. The difference in wing size increases over time, D. Again, the population size goes up.
A. Road kill declines, but the population increases. B. Road kill birds have longer wings than the population at large. C. The difference in wing size increases over time, D. Again, the population size goes up. (From Brown & Brown, 2013, Current Biology)

Wing shape in birds is well known to relate to specific functional abilities, and shorter-winged birds are better at vertical take off and pivoting. The Browns suggest that as the birds moved from their pre-industrial nesting spots (on cliffs) to bridge abutments and highway overpasses, the ability to avoid speeding cars conferred a selective advantage (the swallows frequently land in the road).

The authors acknowledge that other selective factors may influence wing size in the birds, and allow that a decrease in road kills could be due to learning.

[JAC note: one problem here is the lack of demonstration that the changes in wing length really were due to genetic as opposed to purely environmental causes (for example, perhaps temperature changed over the years in a way affecting wing length). A genetic basis for the change is, of course, essential for showing that the short-term change really did reflect evolution. Given that the dead versus live birds did not change in the same direction, however, one can tentatively rule out some environmental factor affecting all birds the same way. Nevertheless, results like these must always remain tentative until genetic work—ideally breeding under constant conditions in captivity—is performed. See Greg’s caveat below.]

This study joins a growing list of observations of evolution-in-action over short time periods in birds. These include the pioneering studies of selective mortality in house sparrows by Hermon Bumpus,  and the now classic, decades-long studies by Peter & Rosemary Grant and their colleagues on Galapagos finches.

Bumpus’ work, which Matthew posted about recently, was one of the very first studies of natural selection, and his data has been much analyzed (see the data, bibliographies, and discussions posted by the Field Museum, Clark University and Pearson College). Like Bumpus’s study (but unlike the Grants, who also had quantitative genetic data), the Browns’ study is of phenotypic selection, and does not demonstrate the genetic basis of the observed changes (although a several millimeter change in wing length begins to approach low-level taxonomic importance).

One unusual aspect of this study is that there appears to be an increase in the size of the population. Sir Ronald Fisher showed 80 years ago that in simple, but fairly general, models of natural selection, the effect of selection is to increase mean population fitness, something he called the “fundamental theorem of natural selection“. In laboratory populations, this is actually not infrequently observed: a newly established population of flies or a culture of bacteria will increase in equilibrium population size or reproductive rate as the population adapts to the new laboratory conditions. But in nature, populations are subject to control by a wide variety of factors (e.g. predators, competitors, climate), so that populations may evolve genetically (increasing their mean “fitness”) without changing in size (because the carrying capacity is set by these other ecological factors). Alternatively, size changes that do occur may be in response to these ecological factors and not to changes in fitness. In the swallows, viability with respect to road kills (a component of fitness) is seen to quite directly increase (i.e., the mortality rate declines), and the population size correspondingly increases. I think it certain that many factors influenced the increase in population size of the swallows, and it would be hard to partition out the effect of decreased car-collision mortality. Nevetheless, in this case an increase in mean fitness due to selection among individuals appears to be reflected in overall population size.

Darwin would, I think, be gratified by all the evidence for evolution by natural selection that has accumulated since the Origin was published in 1859, but I believe nothing would have astounded him more than the now-abundant evidence for evolution occurring on the timescale of a single human life.

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Brown, C. R., and M. B. Brown. 2013. Where has all the road kill gone? Current Biology 23:R233-R234.

Bumpus, H.C. 1899. The elimination of the unfit as illustrated by the introduced sparrow, Passer domesticus. Biological Lectures from the Marine Biological Laboratory Wood’s Holl, Mass. 1898: 209-226. (BHL)

Grant, P.R. and Grant, B. R. 2008. How and Why Species Multiply. The Radiation of Darwin’s Finches. Princeton University Press, Princeton, New Jersey.