Evolvability, speciation, and sex

Self-fertilization sure is convenient, but it spells doom in the long run.

One of the larger questions in evolutionary biology is about the level of natural selection. Dawkins leads the fundamentalists in saying that the level of selection is the gene. Nothing but the gene, ensconced within individuals which live or die by their individual genetic traits. Others, including Stephen J. Gould towards the end of his life, couldn't help but see a wider picture, where species and even genera had distinct high-level traits that are, over long periods of time, weeded out by natural selection.

I am very much in the group selection (also called multi-level selection) camp, seeing selection acting on many levels, from the single nucleotide to genera and kingdoms. The issue isn't whether DNA is the heritable material, (supplemented by culture to some degree among higher animals), and thus the ultimate locus of heritable selection, but whether selection can be thought of coherently as acting on higher levels such as groups whose members share some kind of selectable traits in common, and thus can be differentiated from other groups in the struggle for existence.

Perhaps this is merely a matter of perspective, were the gene fundamentalists emphasize that any change in population frequencies is due to the gain or loss of individuals, (and individual genes), whatever their traits might be that gain expression at higher organizational levels- such as altruism, herd instinct, exogamous mating, tendency to speciate, etc. Group selectionists, in contrast, emphasize the trait rather than the transmission mechanism, see group-level traits as irrelevant on the individual level, and thus see natural selection as irrelevant there also.

At any rate, a recent paper (and review) was a very nice demonstration of a species-level trait with serious consequences- self-fertilization versus self-incompatibility among plants. Most plants produce both male and female gametes (pollen and ovules). Some exceptions (dioecious) come in female and male versions, and example being the date palm. Buying such palms can be a tricky business at a young age, since only the females grow dates, and can't be sexed till they give fruit.

However, most plants produce both male and female gametes, often having anthers and ovules within the same flower. How do they ever manage to mate with other plants? Putting aside macro-physical mechanisms such as having gametes mature at different times, or putting them on different structures on the same plant, or the most glorious mechanism of all- using insects or birds for cross-pollination ... most such hermaphrodytic plants have molecular incompatibility systems, where the "self" pollen grains are recognized when they hit the pistil, and are summarily blocked from germinating or growing down into the ovule.

Molecular incompatibility systems are quite complicated, with proteins expressed on the pollen surface, other protein receptor proteins expressed in the stigma/pistil, multiple variants of each spread through the population, and close genetic linkage between the matching ligand/receptor gene pairs so that the host plant always rejects its own pollen. (Related paper on the intricate system in Petunia.) Such things are difficult to evolve, and easy to lose by mutation.

And lose them they do. This paper starts from the observation that such systems are frequently lost over evolutionary time, creating the fascinating question: why maintain such costly systems of outbreeding, much like the elaborate exogamous-marriage traditions common in tribal societies? The cost for plants is clear- a fortunate plant, dispersed by a helpful squirrel or jay, may find itself far away from its origin, ready to colonize new habitat. But it can't if no pollen wafts its way from a compatible partner. End of story. Some higher animals have developed parthenogenesis for similar reasons of convenience, but finding mating partners is generally easier for mobile animals than for plants, so the issue is less pressing and the trait much less common.

The problem, of course, is that sex is great- it promotes genetic diversity and recombination, allowing bad genes to be combined into loser individuals and good genes into winner individuals. Shuffling genes through all the individuals of a population releases variation rather than confining it to the clones of each self-fertilizing lineage, fated to live or die by the co-lineal sibling genes it is stuck with. Beneficial mutations arise far less frequently than harmful ones, making this clonal restriction a losing proposition. By promoting population-wide recombination and diversity, sex improves adaptation, which is where this paper hangs its hat.

The authors looked at 356 species of the Solanaceae family of plants, (nightshade, potato, tobacco, chili pepper, tomato, etc.), classifying them as self-incompatible or self-fertilizing. This family and its ancestors have maintained self-incompatibility systems with dozens of alleles for ~90 million years, yet continually gives rise to self-fertilizing species as well. These derivatives don't recover self-incompatibility, so this is a one-way street, a ratchet that tests whether there is something about self-incompatibility that is beneficial enough to withstand constant loss of species to the auto-sexual "dark side", as it were.

Looking at a phylogenetic tree of these species, constructed with help from molecular data, (from publicly reported chloroplast genes), the authors derive rates of speciation, and rates of extinction. Actually, a phylogenetic tree is built from extant organisms, so it isn't going to directly provide rates of extinction. The authors derive them by magical (err- mathematical) means via repeated modelling and simulation of similar trees, which I have neither the data nor expertise to assess.

Phylogentic tree of selected Solanaceae, (root starts at 36 million years ago), with self-incompatible (SI) species in purple, compatible (SC) species in blue/turquoise. C diagrams the model of transitions between SI and SC species, with lambda = speciation, mu = extinction, r = net diversification rate. A and B show the deduced relative rates for each process among the species classes. Rates are given in per million years.

To get a feel for what is going on, however, note in the figure that self-fertilizing plants (turquoise) are sprinkled throughout the tree (outside circle) quite evenly. Very few form deep roots that lead to large lineages devoid of self-incompatible species. This is not what you would expect from a frequent one-way process leading to evolutionarily successful self-fertilizing plants. But it is what you would expect from a process that frequently and from the very earliest times gives rise to self-fertilizing plants that then also die out relatively quickly.

Their statistical conclusions are displayed in the graphs (A, B), with lambda as the speciation rate, mu as the extinction rate, C standing for self-compatible, and I for self-incompatible. Lambda-C (yellow) is quite high. Self-fertilizing plants colonize new areas very well, and specialize quickly. However mu-C (grey-blue) is higher still, indicating that those novel self-fertilizing species can't manage to adapt well on the long term, probably because they can not utilize a population-wide reservoir of variation as efficiently as out-breeding plants can. The result (r: the net diversification rate, graph B) is that self-fertilizing species don't hang on for the long term: lower long-term net diversification. Disease might be a particularly difficult challenge, demanding ongoing diversity and recombination in the population to meet the constantly evolving threats from pathogens.

A Dawkensian could construct the finding that inbreeding species do worse on the species level in a gene-based narrative. Individuals in these species are becoming less fit as whatever beneficial mutations they build up are trapped in their parochial lineage, held hostage to whatever other problems that lineage might have. Their gene complements are not keeping up with those of out-crossing species that systematically recombine to join the best of local and even distant variation into better-optimized plants, whose greater accessible population variation likewise serves as a buffer against bad times and unforeseen conditions. In short, outbreeding plants evolve better, though not faster, than their inbreeding congeners.

While such a gene-centric construction would not be wrong and is important to appreciate for a micro-level analysis, outbreeding also seems to be an eminently species-level trait, as is extinction, making a group selection view appropriate as well. The divergent trends of species sharing either fertilization trait creates a conceptual species-level or higher rule that we can see as group trait, by which species live or die, on the very long term. Indeed, for the purposes of variation and adaptation, outbreeding populations form what could be thought of as super-organisms. So sex is good- very good for species, which is why individuals put so much effort into it, pumping out clouds of pollen, luring insects to their lush crevices, and making our world such a colorful and biologically networked place.

• A bit of biological history, in New Zealand.
• Overview episode of mid-empire economics from the outstanding History of Rome podcast.
• Should we use deterrence to prevent crime?
• Case for the carbon tax.
• Get some vitamin D.
• A paper on the cycles of economic history, and Abba Lerner.

"For Lerner inflation that occurred before 3 per cent unemployment was a product of faulty institutions, not a problem inherent in markets. Thus he refused to accept that the target level of unemployment should be raised to whatever level required to stop inflation."

• In a related vein, some economic fallacies, by Vickrey.

"Government debt is thought of as a burden handed on from one generation to its children and grandchildren.

Reality: Quite the contrary, in generational terms, (as distinct from time slices) the debt is the means whereby the present working cohorts are enabled to earn more by fuller employment and invest in the increased supply of assets, of which the debt is a part, so as to provide for their own old age. In this way the children and grandchildren are relieved of the burden of providing for the retirement of the preceding generations, whether on a personal basis or through government programs."

Though I would hasten to add, this applies only in financial terms. In real terms, the older generation gets whatever it needs from the services of the younger, so the savings serve only to make the older generation financially able to demand the requisite services on the market, not magically able to provide directly for themselves. The "payback" is the share of future real production diverted to those who have previously saved into bonds and other assets.