Knee deep in the fetid pools of evolution

I am, as I may have told you before, an evolutionary biologist at heart. And one of the things I love about evolution is how messy, random and complicated it is. Evolutionary outcomes aren't just survival of the fittest, but also reproduction of the luckiest and replication of the not overly deleterious. Natural selection often doesn't get its way and the optimal trait often doesn't exist or can't quite win out. Evolution is a box of dirty tooth-marked mismatched Legos with no instructions all in clumps from previous projects, and that is how I like my Legos

So I always enjoy talking with colleagues who really think about evolution in depth, not as a nice neat optimization process (which it isn't) or a collection of family tree (which it can be, but this misses the forest) but rather as the beautiful mucky anarchic tangled mess of genes, lineages, mutations and highly fallible biology that it is. Sure, there is a lot of phylogeny in there, and a bunch of natural selection, which to an extent can optimize things, but it is like optimizing the design of a boat when all you have to work with is coconut husks, maple syrup and a swarm of fire ants. It isn't so much optimization with constraints as a bowl of constraints with optimized sprinkles on top. To really capture the beauty of it you have to do away with the basically creationist notion that organisms are perfect for their niches and the anarchic view that biology follows the rules we write in text books. Organisms only breed with members of their own species, except when they don't, and clones are genetically identical to each other, unless you look closely.  Only changes to DNA are heritable, except those non-DNA heritable traits. Rules, broadly defined, do not apply to fungi. The dissertation that was defended from me this week showed that in real wild populations, genetic drift is sufficient to speed aging and shorten lifespan. These populations aren't short lived because there is something optimal about it, but rather because drift isn't letting selection have its own way. I'm oversimplifying, and you'll have to wait for the details to come out, but it is a wonderful example of evolution in its slip-shod Rube Goldberg glory.

I'd like spend more time with colleagues who think deeply about the gorgeous multi-layered sub-optimality of evolution. That's where the fun is.

Taxonomically not what you eat

One should be cautious in naming a taxonomic group for their ecological habits.

I offer you these examples:

1. Most turtles are amphibious; all are reptiles, not amphibians. Turtles have scales, lay hard leathery eggs, have the physiological and genetic makeup of reptiles. I often see phrases such as, "turtles and other Amphibians" in writing about biology by non-scientists. The taxonomic term 'amphibians' is not helpful in getting across to people that turtles are reptiles.

2. Consider the Carnivora. Most Carnivora are carnivores, but some, such as the giant panda, eat largely plants. Further, many carnivorous mammals are not Carnivora in the taxonomic sense. Unnecessarily confusing.

3. Pity the poor Insectivora. It turns out things are worse than just dietary nonconformity (not all the Insectivora ate insects, and not all insectivorous mammals were called Insectivora). The group called Insectivora no longer exists! Biologists had assumed that similarities in diet and morphology among the moles, shrews, tree shrews, golden moles, hedgehogs, moonrats, solenodons, tenrecs, elephant shrews and colugos were the result of common descent (they all had these traits because they were all closely related to each other). It is now clear that Insectivora was an ecological rather than taxonomic grouping. This is because modern molecular genetic and phylogenetic methods make clear that most of these Insectivores are not any more closely related to each other than they are to you, or to an elephant. Specifically, the moles, shrews, solodons, hedgehogs and moonrats form one group, whose closest relatives include the carnivores and hoofed mammals. The tree shrews and culogos (of southeast Asia) are more closely related to the primates. The golden moles, tenrecs and elephant shrews (all African groups) are related to larger mammals found in Africa such as the aardvarks and elephants.

4. The Caprimulgidae (Latin for goat suckers), do not suck goats. They were named for a feeding behavior falsely attributed to them. They are in fact insectivores.

A third way of seeing things

The paper I'm writing now is on sex-biased longevity in primates. I'm trying to understand why in some species the males live longer, and in others the females live longer. The story I'm trying to test goes like this:

The largest investment in primates' offspring is in the form of care, not eggs or sperm or pregnancy. In species where females provide all of the care, males need not stay with a single mate, so the operational sex ratio is male biased (i.e. lots of males are out looking for a mate, while most of the females are pregnant or nursing and therefore not looking to mate), reproductive skew is high for males (some males will father lots of offspring, others none), and the fitness rewards to successful male competitors are great. Larger males are more likely to win these competitions, resulting in an increase in optimal male size. These large belligerent males risk increased mortality through conflict, and through diversion of physiological and developmental resources away from longevity and into competitiveness. Simultaneously, selection for longevity in females may be increased by the need to stay alive until their young become independent (and in the case of humans, to care for grandkids). This leads to males who, relative to females, are non-caring, short-lived, large and conflict prone.

I have data (gleaned from the literature) for a bunch of primate species on how long males and females live, how much care the fathers provide in each species, how big males and females are and how frequently and intensely males fight with each other. Depending on how I analyze these data, I get two very different answers. If I treat each species as an independent sample, and look at the correlations between these variables, the data completely support the story. The species range along a continuum having short-lived belligerent large, uncaring males at one end and long-lived caring low-conflict small males at the other.

But most evolutionary biologists would say that is not the right way to analyze the data. I need to take into account the relationships among the species. Two traits might seem to be correlated not because the one makes the other selectively advantageous, but because a group related species all have the one and all have the second. Take the example of feathers and laying eggs. All birds have feathers and all birds lay eggs. Is this because something about feathers requires egg-laying (probably not) or because all birds are descendents of some ancestral birds that laid eggs and had feathers, and ever since no bird has arisen that didn't do both those things. That all birds have eggs and feathers is an example of what biologists call evolutionary inertia.

The question this poses for me in writing my paper on primates is whether the correspondence between sex-biased longevity and these other variables is because of the adaptive story I told you, or because of evolutionary inertia. So I look at the data a second way, and see that there is a great deal of evolutionary inertia in these traits. Most primate species are somewhere near the middle of that continuum I described. Ever species at one end is from one group of related monkeys. Every species at the other end of the continuum is either a great ape or from a different family of monkeys. Plugging my data into software designed to test for evolutionary inertia, I find that closely related species are very likely to have similar values for all the traits I am measuring, and that inertia is fully sufficient to explain the correlations between these traits. It is like eggs and feathers in bird.

As I am trying to write the paper to present all of this in a scientifically rigorous way, I am struggling with what to say about it. The easiest, and least interesting, conclusion would be to simply say that the correlations are purely illusions conjured by evolutionary inertia. What I'm attempting to find a way to argue it that it could just be inertia, but that the inertia might be because of selective effects. In other words, that both the inertia story and the selective story could simultaneously be true, and closely related species are similar not because they can't change, but because what was adaptive for their common ancestor is still adaptive for them. If a male from a very belligerent species was to grow in a way that made him not a good competitor, but able to live a long time and provide care to his young, this wouldn't fit with the way his species lives, so he wouldn't pass on his novel trait, and his species would stay like their ancestors had been. It is evolutionary inertia caused by adaptive mechanisms. I think my next step is to find out who has already written about adaptive evolutionary inertia, and what they said.

Phylogeny schmylogeny

Phylogenetics-
1. The generating and using of increasingly complex guesses as to how organisms are related to each other.
2. Something you have to do these days to study evolution.

That time has come. For five years in a heavily phylogenocentric lab in a museum mostly focussed on phylogeny in a department deeply into phylogenetics at a time when phylogenetics is nearing (I hope) the zenith of its trendiness, I have avoided really learning how to do phylogenetics. I can talk at length and in detail about the philosophical underpinnings of phylogenetics, I have read books and papers and taken classes on the subject, but I have never actually sat down and applied that knowledge. This is partly because of my inherent and unreasonable dislike for everything trendy and partly because I find that the most boring research talks in the universe are the straight phylogeny talks ("And then we sequenced 4327 base pairs of CR32.5 and SLD19423 from these twelve hundred taxa. Notice that on this taxa here there is a deletion, and I'll spend ten minutes talking about how we dealt with that. Now I'll spend half an hour talking about how we generated the priors for our Baysian analysis. And look, this taxon you have never heard of is closely related to this other taxon you have never heard of. Who would have thunk it? Someone wake that guy with the funny hair").

But my phylogenetic inexperience is based on more than simple obstinacy. I don't think that way. My predilection is to think of evolution in terms of selection, mutation, drift and so on. Phylogenetics at its core doesn't care WHY there are differences between organisms, phylogenetics is focussed on the methods for gathering and analyzing data on HOW these taxa are different from each other, and on drawing trees of relationships. In many papers, the tree itself is the goal, and maybe they do an analysis or two showing how useful their tree is.

I, knowing I needed to learn some phylogenetic software packages eventually, but deeply not wanting to, have backed myself into it. So I have taken a taxon for which the tree already exists (primates) and gathered from the literature (or had my students gather) a bunch of variables for as many species on that tree as possible. We have data on sex biased dispersal, social system, who provides care to the young and so on for about 90 species, and data on sex-biased longevity for 119. A huge amount of work over some years has gone into this, and there is no way I can weasel out of writing papers based on it. But there is also no way I can publish this in a decent journal without controlling for the effect of phylogeny. What "controlling for the effect of phylogeny" means takes a little bit of explaining. There is a tendency for related species to have similar traits, whether or not there is any adaptive mechanism driving that similarity. The common ancestor had that trait and both the descended populations inherited that trait from that ancestor. Humans and chimps have similar genetic sequences, and our common ancestor was surely very similar to both of us. This is termed 'phylogenetic inertia.'
Anytime one does a comparative analysis these days, one has to explain how we know that the observed pattern isn't just an example of phylogenetic inertia. Imagine one thought there was a causal relationship between being large and having hooves. One could find ten big species, notice they all have hooves, and ten species, notice none of them have hooves. But if those ten hooved species were all in the cow family, and the ten small species were all in the vole family, one would not have proved anything about hooves and largeness except that Bovidae have both and Cricetidae neither. So one has to make sure one is not being fooled by similarities due to evolutionary relatedness, or in the parlance, 'control for phylogeny.'
I need to control for phylogeny, and therefore will learn a few phylogenetics programs. But I don't have to like it, and I am going to make my students learn it too.

phylogenetic inertia and cooperative breeding

I spent yesterday evening reading the literature on the extent to which there is phylogenetic inertia (the tendency for related species to have similar traits because they both inherited those traits from the common ancestral population) in cooperative breeding (the habit of having more than two individuals caring for the young).

My general conclusions are:
1. A species whose relatives are cooperative breeders are often cooperative breeders themselves.
2. It is not entirely clear if cooperative breeding itself is phylogenetically conserved in many groups, or if the traits that make it a useful strategy are conserved, leading to the impression of inertia in the evolution of cooperative breeding.
3. Phylogenetists spend a lot of time and ink poodling on about the flaws in each other's methods, but always end by saying that the conclusion about the trait is probably robust to minor variations in the shape of the tree.
4. Cooperative breeding is a blanket term for several different phenomena, and papers that deal with this explicitly are more convincing than those that only pay it lipservice.
5. The data I am already putting together on who provides how much care in 120 primate species could probably also be used for a very useful paper on phylogenetic inertia in cooperative breeding.