The natural selection of altruistic traits

Proponents of the standard evolutionary biology paradigm explain human “altruism” in terms of either nepotism or strict reciprocity. On that basis our underlying nature is reduced to a function of inclusive fitness: human nature has to be totally selfish or nepotistic. Proposed here are three possible paths to giving costly aid to nonrelatives, paths that are controversial because they involve assumed pleiotropic effects or group selection. One path is pleiotropic subsidies that help to extend nepotistic helping behavior from close family to nonrelatives. Another is “warfare”—if and only if warfare recurred in the Paleolithic. The third and most plausible hypothesis is based on the morally based egalitarian syndrome of prehistoric hunter-gatherers, which reduced phenotypic variation at the within-group level, increased it at the between-group level, and drastically curtailed the advantages of free riders. In an analysis consistent with the fundamental tenets of evolutionary biology, these three paths are evaluated as explanations for the evolutionary development of a rather complicated human social nature. This paper (in a series of drafts) has profited from comments by Michael Boehm, Donald T. Campbell, Bruce Knauft, Jane Lancaster, Martin Muller, Peter J. Richerson, Gary Seaman, Craig Stanford, George Williams, Edward O. Wilson, David Sloan Wilson, and two reviewers for Human Nature. Christopher Boehm is a professor of anthropology and the director of the Jane Goodall Research Center, University of Southern California. His research interests in political anthropology concern egalitarianism, feuding, warfare, and conflict resolution (humans and chimpanzees). In biosocial anthropology he is interested in altruism, group selection, and decisions.     

The negative view of natural selection

An influential argument due to Elliott Sober, subsequently strengthened by Denis Walsh and Joel Pust, moves from plausible premises to the bold conclusion that natural selection cannot explain the traits of individual organisms. If the argument were sound, the explanatory scope of selection would depend, surprisingly, on metaphysical considerations concerning origin essentialism. I show that the Sober-Walsh-Pust argument rests on a flawed counterfactual criterion for explanatory relevance. I further show that a more defensible criterion for explanatory relevance recently proposed by Michael Strevens lends support to the view that natural selection can be relevant to the explanation of individual traits.     

The fundamental theorem of natural selection

R. A. Fisher's Fundamental Theorem of Natural Selection states that the rate of increase in the mean fitness of a population ascribable to gene-frequency changes is exactly equal to the additive genetic variance in fitness. It has been widely misunderstood, though clarification has gradually come about particularly through the work of G. R. Price, W. J. Ewens, and S. Lessard. Building on their interpretations we here explain the approach adopted by Fisher (1941), devising a figure as an aid to understanding this important paper.     

The role of natural selection in evolution

To evaluate properly a role of natural selection, its effect should be considered in relation to different phases of the evolutionary cycle postulated earlier by the author. At the first stage of the cycle natural selection is directed towards organism's persistence to detrimental external factors and leads to an increased fitness (that is viability and fecundity) in every generation. At the next stage of the cycle natural selection occurs under conditions of intraspecific competition and is directed towards a more efficient utilization of food resources. At this stage natural selection leads to formation and divergence of intraspecific races and is carried out by "single" selection actions occurring now and then and consisting of the survival of rare mutants with an altered ecological potential. Such a strict selection for certain mutants occurs again during the periods of acute competition for food, the selected mutants being characterized by a decrease of fitness, the latter to have been restored by means of the "ordinary" selection within the intervals between crises. According to the model suggested, homozygotes for "detrimental" recessive alleles could be selected in diploids, as the mutants mentioned with altered ecological potential. At the end of the cycle, there is a kind of selection for hybrids in which ecological potential of specialized intraspecific races is combined. The genetic drift is considered as an inevitable consequence of the postulated mechanism of natural selection.     

The non-existence of a principle of natural selection

The theory of natural selection is a rich systematization of biological knowledge without a first principle. When formulations of a proposed principle of natural selection are examined carefully, each is seen to be exhaustively analyzable into a proposition about sources of fitness and a proposition about consequences of fitness. But whenever the fitness of an organic variety is well defined in a given biological situation, its sources are local contingencies together with the background of laws from disciplines other than the theory of natural selection; and the consequences of fitness for the long range fate of organic varieties are essentially applications of probability theory. Hence there is no role and no need for a principle of the theory of natural selection, and any generalities that may hold in that theory are derivative rather than fundamental.     

The incidental response to uniform natural selection

When populations are exposed to novel conditions of growth, they often become adapted to a similar extent, and at the same time, evolve some degree of impairment in their original environment. They may also come to vary widely with respect to characters which are uncorrelated with fitness, as the result of chance genetic associations among the founders, when these are a small sample from a large and variable ancestral population. I report an experiment in which 240 replicate lines of the unicellular chlorophyte Chlamydomonas were derived from primarily photoautotrophic ancestors and cultured as heterotrophs in the dark. All adapted to the dark and were impaired in the light after several hundred generations of culture. They also displayed a wide range of colony morphologies that were uncorrelated with fitness. This incidental response to selection probably arose through random variation in the initial composition of the lines. The differences between closely related species or varieties may likewise arise, in similar circumstances, by sampling error rather than natural selection.     

The meaning of natural selection revisited at the molecular level

Various molecular interaction mechanisms cause biased transmission of genes. Meiotic drive is an example of strong bias, and compartmentalization of mammalian chromosomes reflects weak bias. Such biases are the results of interaction between DNA and proteins, and should be distinguished from natural selection. Separating the effects of molecular interaction from those of natural selection, however, is often very difficult. Natural selection and molecular mechanisms interact, and our understanding of how selection works requires revision.     

The origin of autonomous agents by natural selection

We propose conditions in which an autonomous agent could arise, and increase in complexity. It is assumed that on the primitive Earth there arose a recycling flow-reactor containing spontaneously formed oil droplets or lipid aggregates. These droplets grew at a basal rate by simple incorporation of lipid phase material, and divided by external agitation. This type of system was able to implement a natural selection algorithm once heredity was added. Macroevolution became possible by selection for rarely occurring chemical reactions that produced holistic autocatalytic molecular replicators (contained within the aggregate) capable of doubling at least as fast as the lipid aggregate, and which were also capable of benefiting the growth of its lipid aggregate container. No nucleotides or monomers capable of modular heredity were required at the outset. To explicitly state this hypothesis, a computer model was developed that employed an artificial chemistry, exhibiting conservation of mass and energy, incorporated within each individual of a population of lipid aggregates. This model evolved increasingly complex self-sustaining processes of constitution, a result that is also expected in real chemistry.     

The question of natural selection against mutable-to-terminator codons

Codons that differ from a terminator triplet by only a single base are sometimes thought, because of their greater risk of undergoing a harmful mutation, to be kept at a reduced frequency by natural selection. The present study on human genes shows that these codons are infrequent, but their low frequency is not directly related to their risk of mutation to terminator. Rather, it is a consequence of their ending in A or G; comparable A-ending and G-ending codons that are not mutable to terminator are also infrequent. Natural selection does not appear to have depressed the frequency of mutable-to-terminator codons by directly eliminating some of them individually. It may have depressed their frequency indirectly by adjusting mutation rates in the population so that most of the purine-ending codons--and consequently most of the mutable-to-terminator ones as well--are infrequent.     

The effect of natural selection on the performance of maximum parsimony

Background  

Maximum parsimony is one of the most commonly used and extensively studied phylogeny reconstruction methods. While current evaluation methodologies such as computer simulations provide insight into how well maximum parsimony reconstructs phylogenies, they tell us little about how well maximum parsimony performs on taxa drawn from populations of organisms that evolved subject to natural selection in addition to the random factors of drift and mutation. It is clear that natural selection has a significant impact on Among Site Rate Variation (ASRV) and the rate of accepted substitutions; that is, accepted mutations do not occur with uniform probability along the genome and some substitutions are more likely to occur than other substitutions. However, little is know about how ASRV and non-uniform character substitutions impact the performance of reconstruction methods such as maximum parsimony. To gain insight into these issues, we study how well maximum parsimony performs with data generated by Avida, a digital life platform where populations of digital organisms evolve subject to natural selective pressures.     

The measurement of stable isotope natural abundance variations

Precise stable isotope natural abundance analysis of the elements of organic matter, yields a wealth of information for the biologist. Robust sample preparation methodology and analytical instrumentation is necessary to achieve precise results. Basic principles of isotope ratio mass spectrometry (IRMS) are detailed, with particular regard to sample size, gas production and transfer into the IRMS ion source. Gas preparation methods developed to give quantitative yields of pure simple gases from organic and inorganic materials include vacuum line combustion, ampoule combustion and automated elemental analysers used off and on-line. The new technique of GC-C-IRMS, where individual volatile organic compounds are separated by GC, combusted and analysed on-line by IRMS, is also described. The conventional dual batch inlet developed by geochemists for the most precise analysis of stable isotopes, is contrasted with continuous flow-IRMS analysis. The needs of the biological scientist for rapid throughput of small samples are discussed in this context. It is argued that the development of new instrumental approaches will permit many new applications of stable isotope methodology in the biological sciences.     

Maladaptation and natural selection

The transformations George Williams initiated in evolutionary biology seem so blindingly obvious in retrospect that they spur the question of why he saw what no one else did. While most humans are prone to see only what theory predicts, Williams sees in bold relief whatever does not fit. Not an adaptationist or an anti-adaptationist, Williams is better described as a maladaptionist. The challenge of finding evolutionary explanations for apparent maladaptations has been overlooked with casualness akin to that once typical for group selection. Suboptimal traits tend to be dismissed as illustrations of the weakness and stochastic nature of selection compared with mutation and drift. A closer look suggests that such constraints are only one of six possible kinds of explanations for apparently suboptimal designs: mismatch, coevolution, tradeoffs, constraints, reproductive advantage at the expense of the individual, and defenses that are aversive but useful Medicine has asked proximate questions at every possible level but has only begun to ask evolutionary questions about why bodies are vulnerable to disease. Considering all six possible evolutionary reasons for apparently suboptimal traits will spur progress not only in medicine but also more generally in biology. 'Williams Vision" may not yield a net benefit to the possessor, but it is invaluable for the species.     

Limits to natural selection

We review the various factors that limit adaptation by natural selection. Recent discussion of constraints on selection and, conversely, of the factors that enhance "evolvability", have concentrated on the kinds of variation that can be produced. Here, we emphasise that adaptation depends on how the various evolutionary processes shape variation in populations. We survey the limits that population genetics places on adaptive evolution, and discuss the relationship between disparate literatures.     

Grandmothering and natural selection

Humans are unique among primates in that women regularly outlive their reproductive period by decades. The grandmother hypothesis proposes that natural selection increased the length of the human post-menopausal period—and, thus, extended longevity—as a result of the inclusive fitness benefits of grandmothering. However, it has yet to be demonstrated that the inclusive fitness benefits associated with grandmothering are large enough to warrant this explanation. Here, we show that the inclusive fitness benefits are too small to affect the evolution of longevity under a wide range of conditions in simulated populations. This is due in large part to the relatively weak selection that applies to women near or beyond the end of their reproductive period. However, we find that grandmothers can facilitate the evolution of a shorter reproductive period when their help decreases the weaning age of their matrilineal grandchildren. Because selection favours a shorter reproductive period in the presence of shorter interbirth intervals, this finding holds true for any form of allocare that helps mothers resume cycling more quickly. We conclude that while grandmothering is unlikely to explain human-like longevity, allocare could have played an important role in shaping other unique aspects of human life history, such as a later age at first birth and a shorter female reproductive period.