The Evolution of Spite (and Altruism)

Behaviors that decrease the relative fitness of the actor--and also either benefit (altruism) or harm (spite) other individuals--are difficult to reconcile with natural selection and maximization of individual fitness. The paragon of altruism is the sterile worker caste within eusocial insect colonies, which help rear the offspring of their queen, or the slime mold cells that altruistically give up their own survival to become the nonviable stalk of a fruiting body, helping other cells to disperse in the form of spores. These behaviors reduce the reproductive success of the altruist--so why doesn't natural selection weed out the genes responsible for such behaviors?


Hamilton showed that genes can spread not only through their direct impact on their own transmission, but also through their indirect impact on the transmission of copies present in other individuals. He introduced the theoretical concept of inclusive fitness--Hamilton's Rule--which states that a trait will be favored by selection when rb-c>0, where c is the fitness cost to the actor, b is the fitness benefit to the recipient and r is their genetic relatedness. Consequently, altruistic behaviors are favored if the benefits are directed toward other individuals who share genes for altruism.


Eusociality, depending on how it is defined, has evolved 3-11 times in Hymenoptera (ants, bees, wasps), termites, thrips, aphids, spiders, beetles, shrimps and mole rats. A crucial parameter necessary for the evolution of eusociality is strict, one-time monogamy (which has been shown as the ancestral state in all independent origins of eusociality studied), in which females only mate one male in their entire life. This monogamy leads to a potential worker being equally related (r=0.5) to her own offspring and to the offspring of her mother (siblings). In this case, any small efficiency benefit for rearing siblings over their own offspring (b/c>1) will favor eusociality (such benefits include life insurance=helpers completing parental care after the death of the mother, as well as fortress defense=help use or defend a food source when opportunities for successful migration are low). Later in evolutionary trajectories of eusocial animals, once the workers have lost the ability to mate and realize full reproductive potential themselves and generally have specialized to a division of labor that gives a substantial b/c (a large efficiency benefit for sibling-rearing since siblings are less related to the individual than their own offspring would be), some queens develop the ability/behavior to mate with multiple males.


Spiteful behaviors would be favored--i.e. rb-c>0 is satisfied--if c is positive (which is costly to the actor) and b is negative (which is costly to the primary recipient of the spiteful behavior), only if relatedness between the actor and recipient, r, is negative (negative relatedness is when the recipient is less related to the actor than expected by chance). The indirect fitness of spite is that secondary recipients, more closely related to the actor than the primary recipient, experience reduced competition from the primary recipient harmed by the spiteful behavior. Spite is therefore altruism to the secondary recipients: harming an individual is favored if it provides a benefit closer relatives.


Some confusion about spite arose due to certain behaviors only being evaluated with respect to direct fitness over the short term rather than over the lifetime of the actor; these include bird siblicide at neighboring nests and fish egg cannibalism (decreased competition for resources for the actor and/or actor's offspring), mammalian infacticide, especially of juvenile males (decreases competition for offspring or mates) and human punishment/rejection of low offers in economic games (increased cooperation over the long term). All of these examples are selfish behaviors that are costly to the recipient but provide a benefit to the actor (c<0). The specific conditions required to favor evolutionary spite, population structures in which harming non-relatives is an efficient way of helping relatives, may be rare in general and unlikely in humans and other primates.


An example of spite can be found in the polyembryonic parasitoid wasps.  A female wasp lays eggs on moth caterpillars, after which the wasp eggs divide asexually into many larvae and consume the growing caterpillar from the inside. Most larvae develop normally, but a fraction become soldier morphs. Developing as a soldier is costly to the actor (they are sterile) and costly to the primary recipient (soldiers seek out and kill larvae that developed from the other eggs within the host), however it is beneficial to the soldier's clone-mates that developed from the same egg, freeing up resources (the caterpillar body) for their consumption.

From a theoretical perspective, spite is plausible if there is large variance in relatedness between competitors, kin discrimination (with harming behaviors aimed at individuals to whom the actor is relatively unrelated), and strong local competition so that harming the primary recipient provides appreciable benefits to the secondary recipients.  Local competition for resources typically selects for spite and against altruism; altruistic traits show a positive, monotonic relationship to relatedness, whereas spiteful traits show a domed relationship; kin discrimination is key for spite, whereas altruism can often evolve without kin discrimination when limited dispersal keeps relatives together.

As Hamilton has pointed out, the indirect fitness benefits derived from altruism and spite require genetic relatedness per se, not kinship (ie. genetic relatedness at the altruism locus, not geneaological relationship over the whole genome). This can be accomplished in two ways: a gene or set of tightly-linked genes that both cause the cooperative behavior and cause cooperators to associate (coined "greenbeards" by Dawkins) or by geneaological kinship. In the slime mold, Dictyostelium discoideum, individuals with the csa gene adhere to each other in aggregation streams and cooperatively form fruiting bodies while excluding noncarriers of the gene. A spiteful greenbeard in fire ants, Solenopsis invicta, is the b allele of the Gp-9 gene, which enables workers to use oder to determine whether prospective queens also carry this allele, dismembering them if they do not.

There are four categories of greenbeards: altruistic and always expressed (obligate), altruistic and only expressed in response to presence of greenbeard in others (facultative), spiteful and obligate, spiteful and facultative.  For all cases except altruistic facultative, the greenbeard is selected against at low frequencies and only favored when it has established itself to a certain frequency. Population structure can solve this problem by keeping individuals with greenbeards together. Some models for altruism in humans implicitly invoke greenbeard mechanisms (suggesting altruistic individuals differ from non-altruistic individuals in some observable characteristic like smiling or tendency for punishment), which is only true if the greenbeard mechanism is encoded by the same gene or closely linked genes as those that lead to the altruism, otherwise falsebeards could too easily arise and the altruism (and its detection) would not be evolutionarily stable.

Microbes are ideal model organisms to look for new greenbeards because their asexual growth leads to extreme population structuring, the genotype is relatively simply linked to the phenotype and this simplicity may prevent decoupling between the greenbeards and falsebeards (cheats that displayed the signal without also performing the behavior), and genetic knockouts can be designed to aid in the detection of greenbeards.  

Another example of spite is the costly production and release of antimicrobial bacteriocins, toxins that can kill unrelated strains of the same species that lack the specific immunity gene. In some cases, cell death is required to release the bacteriocins into the environment, so it is clearly costly to the actor. The bacteriocin production genes are genetically linked to the immunity genes so that close relatives both produce it and are immune to it. When one bacteria does release its bacteriocin, it will thus only kill non-relatives and free up resources for clone-mates.


In the Hawlena study, two natural populations of Xenorhabdus bacteria are carried by entomopathogenic nematodes, dispersing over a range of a few metres within these symbiotic hosts, and use bacteriocins as weapons. The authors found that genetic relatedness decreased and the probability of bacteriocin-mediated (i.e. spiteful) interactions increased with spatial distance between isolates. Measurements were taken at a scale ranging from 1 to 120 metres. Whilst this work has only been done on a relatively small scale and in one system, it is clearly important to test theoretical results with real systems and, fortunately, in this case, the experimental results support the theory.

Hamilton WD. (1963) The Evolution of Altruistic Behavior.  American Naturalist. 97:354-6.


Wloch-Salamon DM, Geria D, Hoekstra RF, deVisser JAGM. (2008) Effect of dispersal and nutrient availability on the competitive ability of toxin-producing yeast. Proc R Soc Lond B. 275:535-41


Hawlena H, Bashey F, Lively CM. (2010) The Evolution of Spite: Population Structure and Bacteriocin-Mediated Antagonism in Two Natural Populations of Xenorhabdus Bacteria. Evolution.


West SA, Gardner A. (2010) Altruism, Spite, and Greenbeards. Science. 327:1341-1344.

How Exactly Do Bacteria Cope with Rapid Environmental Change?

Bacterial DNA replication is generally extremely accurate; however, spontaneous mutants may have increased fitness due to new beneficial proteins (traits) that may be selected for in a rapidly changing environment.  The contribution of post-replication processes to genetic variation has not be examined rigorously and thus transcriptional and translational fidelity (or lack thereof...) has been underappreciated in bacterial selection, and may even be an in-built strategy used by biology to increase protein variation at the single cell level to ensure bacterial robustness under rapid environmental change.


Using a new method for quantifying errors in gene expression at the single cell level in the bacterium Bacillus subtilis, Meyerovich and colleagues reveal that the transcription and translation machinery does not strictly follow the DNA code.  The new method relies on the mutation of a chromosomally encoded green fluorescent protein (GFP) reporter allele, containing frameshifts and premature stop codons, so that errors in gene expression result in the formation of GFP, which would then be observable via imaging of single cells in real time.  Using this method, the authors show that errors in decoding the DNA sequence occur around 1% of the time.  This error rate is at least ten times higher than previous estimates.  Furthermore, the frequency of errors increases markedly in response to certain environmental conditions such as nutrient deprivation (stationary phase), lower temperatures, and toxic accumulation.  The implications are that many individual protein molecules contain potentially significant variations from the encoded amino acid sequence, and that this could increase survival in fluctuating environments or in response to sudden stress.  Consistent with this increased protein plasticity for rapid adaptation, gene-expression errors could combine with a genetic mutation in one gene, allowing the organism to bypass the need to undergo two independent mutations simultaneously. It is unclear whether this error rate increase is due to energetic constraints--the bacteria can't afford error correcting mechanisms under such conditions--or if the bacterial genetic code is selected as a consensus sequence from which protein production generates useful variations.


For any organism, the amount of errors represents a compromise between a cost of dysfunctional proteins and a payoff of beneficial variants that lead to increased phenotypic heterogeneity.  It is likely that evolutionary pressure that shapes codon usage would allow different genes to be prone to unequal error rates according to their cellular function.


Visualizing high error levels during gene expression in living bacterial cells.
Meyerovich M, Mamou G, Ben-Yehuda S.  Proc Natl Acad Sci U S A 2010 Jun 22 107(25):11543-8

The Bare Skin Hypothesis

A paraphrase of the hypothesis offered by Professor Nina G. Jablonksi:

Starting 3 million yrs ago, earth entered into a phase of global cooling that had a drying effect in East and Central Africa, where our human ancestors lived. The decline in regular rainfall changed woodlands into open savanna grasslands. The dwindling resources of fruits, leaves, tubers and seeds as well as drinking water forced our ancestors to abandon leisurely foraging habits for sustained activity of walking/running many miles to stay hydrated and obtain enough calories. Around this time, hominids also began incorporating meat into their diet, as revealed by the appearance of stone tools and butchered animal bones around 2.6 million yrs ago.

Homo ergaster evolved essentially modern body proportions that would have permitted prolonged walking/running and details of the joint surfaces of the ankle, knee and hip make clear that these hominids actually exerted themselves in this way.  The increase in walking and running builds up heat internally in the muscle and would have required that hominds both enhance their eccrine sweating ability (2-5 million watery glands close to skin surface that can produce up to 12 liters of sweat a day, rather than oily apocrine and sebaceous glands associated with deeper hair follicles, all of which develop from the same unspecialized epidermal stem cells) and lose their body hair to avoid overheating in the hot open savannas.  This combination of naked skin and watery sweat that sits directly atop it rather than collecting in the fur allows humans to eliminate excess heat very efficiently.  For furry animals, the effectiveness of cooling diminishes as an animal's coat become wet and matted with this thick, oily sweat.  Under conditions of duress, heat transfer is inefficient (evaporation occurs at the tips of the fur rather than the surface of the skin), requiring that the animal drink large amounts of water, which may not be readily available, in which case, the animal will collapse from heat exhaustion.  Human cooling system is so superior that in a marathon on a hot day, a human could outcompete a horse.  

MC1R gene is one of the genes responsible for producing skin pigmentation.  A specific gene variant always found in Africans with dark pigmentation originated ~1.2 million years ago.  Early human ancestors are believed to have had pinkish skin covered with black fur, much like chimps, so the evolution of permanently dark skin was a presumed requisite evolutionary follow-up to the loss  of our sun-shielding body hair.  

Comparison of human and chimp DNA reveals that one of the most significant differences are in the genes that code for proteins controlling properties of the skin (waterproofness, scuff-resistance).  The outermost skin layer--the stratum corneum of the epidermis--is composed of flattened, brick-like dead cells--corneocytes--which contain a unique combination of proteins, including novel types of keratin and involucrin, and are surrounded by ultrathin layers of lipids that act like mortar. Most genes directing SC development are ancient and highly conserved among vertebrates, so the human mutations signify that they were important to survival.

Maintenance of hair in armpits and groins despite loss elsewhere must serve to propagate pheromones (chemicals that serve to elicit behavioral responses from other individuals) and to help keep these areas lubricated during locomotion.  Hair on the head was most likely retained to help shield against excess heat on the top of the head (a barrier layer of air between sweating scalp and hot surface of the hair, with tightly curled hair being the optimum for max thickness of this airspace).  Other hairtypes/body types evolved as humans dispersed out of tropical Africa.

Daniel E. Lieberman and Dennis M. Bramble. (2007) The Evolution of Marathon Running: Capabilities in Humans.  Sports Medicine 37(4-5): 288-290.

Alan R. Rogers, D. Iltis, S. Wooding. (2004) Genetic Variation at the MC1R Locus and the Time since Loss of Human Body Hair.  Current Anthropology, 45(1): 105-108.

Multicellular life is older than we thought, by 200 million years!

Newly uncovered amorphous fossils from black shale formations of the Francevillian Basin in Gabon, Africa hint that multicellular life may have evolved more than 2 billion years ago -- some 200 million years earlier than previously expected, according to a study published last week in Nature.  A. El Albani, et al., "Large colonial organisms with coordinated growth in oxygenated environments 2.1 Gyr ago,"Nature, 466:100-4, 2010.

Sedimentologist Abderrazak El Albani of the University of Poitiers in France and his colleagues discovered more than 250 specimens at the site, all dating to approximately 2.1 billion years ago, and ranging up to 12 centimeters in length. Chemical analyses confirmed the biological origin of the fossils, which are now composed of the iron-sulfide mineral pyrite that replaced the organic tissue as the organism decomposed. Interestingly, these fossils appear just a couple million years after the Great Oxidation Event, when oxygen became more widely available in the atmosphere and in the shallow oceans. This may have facilitated the evolution of a thicker organism (cells in the middle have greater difficulty obtaining oxygen if it's only at trace levels in the atmosphere). And their large and complex structures, as revealed through X-ray microtomography, are indicative of cell-to-cell signaling and coordinated growth between cells.  Specifically, the fossils display scalloped edges with radiating slits, and many have a central structure, not unlike the overall structure of a jellyfish medusa.  Unfortunately, the insides are not preserved, so it is hard to prove multicellularity, but their size, complexity and organization of structure indicate multicellularity.  Of course, there is debate on the definition of multicellularity itself, as the molecular machinery for cell-to-cell communication is found in more primitive organisms like bacterial colonies.

Unfortunately, according to one of the authors, there aren't many other fossils of that age to corroborate the connection (most of the rocks of that time have been destroyed, and the ones remaining are not pristine enough to find delicate fossil structures).  Why?  Is this due to mining?  It's a shame.  Regardless, it's important to realize that although these may be the oldest known multicellular organisms, multicellularity has evolved at least 20 times even among living lineages and thus, these are not necessarily the ancestors of all multicellular life.

Who's gonna live the longest?

Extreme longevity is associated with a select group of genetic markers, according to a new study of centenarians, people living at least 100 years. Using these markers, researchers can predict a person's ability to become a centenarian with 77 percent accuracy.


The study chose 1000 non-related Caucasian centenarians and super-centenarians (those living 110 years or longer) from the New England Centenarian Study, which has been following people since 1995. The centenarians were compared to younger Caucasians with similar genetic backgrounds.

The researchers compared the frequency of 300,000 single-nucleotide polymorphisms (SNPs) in both groups, then looked for the SNPs that appeared most unique to the centenarians. They sequentially added additional markers down the line, increasing the specificity and sensitivity of the prediction algorithm until the results plateaued. Ultimately, the algorithm contained 150 SNPs that predicted a person's chances of reaching 100 with 77 percent accuracy.

The team is developing a software program for use by other researchers, companies, and individuals to analyze a genetic sequence and determine the likelihood of extreme longevity.

Less than half of the SNPs were located in areas associated with functioning genes. Some linked to the insulin pathway, some to genes associated with Alzheimer's disease (including the ApoE4 gene variant, which is a genetic risk factor for the disease) and dementia. Many of the SNPs point to more basic biological processes, such as chromosomal instability, muscle function and control of the immune system.

Of course, the researchers could only compare centenarians to younger controls, some of whom may eventually become centenarians themselves. However, given that it is such a rare trait -- only one in six thousand people reaches 100 or older -- the researchers said this potential confounder likely had minimal impact on the findings.

The centenarians were placed into smaller groups based on their SNP profiles. Some of the groups showed special characteristics, like those who survive the longest or those with the most delayed onset of age-related diseases. There was one cluster of centenarians that did not carry many of the SNPs associated with longevity. These could be people who lived really healthy lives, or harbor rare variants linked to longevity, the authors suggested.

Even though the centenarians survived so long, the researchers found that they have similar levels of a large set of disease-associated genetic risk factors as the controls, including risk factors for Alzheimer's, diabetes, and cardiovascular disease. This seems to indicate that long-life indicators also somehow mask disease traits.
P. Sebastiani,N Solovieff, A Puca, SW. Hartley, E Melista, S Andersen, DA. Dworkis, JB. Wilk, RH. Myers, MH. Steinberg, M Montano, CT. Baldwin, TT. Perls. "Genetic signatures of exceptional longevity in humans,"ScienceExpress, July 2010.

There is an online calculator that says I will live to 94, like my maternal grandmother!  And if I worked less and gave up coffee, that would probably increase by a number of years...I really need to do 23andme and check out my SNPs.  Let me know if you hear of any future deals with them! 

Science...It works, Bitches!

It's time to finally put aside the car religious fish symbols and the darwinian fish with feet.  Recent work is elucidating one of the crucial juicy mysteries in evolutionary biology: how did fins become limbs?


Published online at Nature, a team of researchers describe 2 proteins essential to fin development in bony fishes and the loss of which may have been a key step in the evolution of tetrapods (4-legged vertebrates).  During a routine screen for genes involved in fin regeneration in the zebrafish labs of Marie-Andree Akimenko and Marc Ekker at the University of Ottawa in Canada, the team noted a remarkable pattern among two of many unknown genes revealed by the screen: a unique and specific localization along the early median fin fold, which runs along a fish's back, and in the pectoral fin buds, fins that grow on each side of the fish's body behind the gills.  This gene expression pattern suggests the proteins are structural components of actinotrichia, the thin, rigid fibrils that form the scaffold of developing bony fins.  The team named the proteins actinodin 1 and 2 (And1, And2) and noted that along with related genes from a database, and3 and and4, were entirely absent in tetrapods.


Using morpholinos (molecules that transiently silence gene expression) to knock down these genes, and1 and and2, the team discovered that the genes are partly redundant, but necessary for fin formation.  If only one of the genes was knocked down, fin development was normal.  However, if both genes were knocked down, actinotrichia didn't form and thus there was no regional recruitment of mesenchymal cells (fin bone precursors).  Other gene expression patterns important for fin patterning in the region were also extensively disrupted during the double knockdown, including those for fibroblast growth factor and sonic hedgehog.  Interestingly, the knockdown gene expression profile in the zebrafish, is highly similar to experimental chick and mouse mutants called Gli3, which results in polydactyly (the presence of numerous extra digits).  Even more noteworthy, one of the earliest aquatic tetrapods, Acanthostega, had 8 digits on each hand, which may indicate that loss of actinotrichia in ancestral tetrapods may have been conducive to limbs resembling polydactyly.


Their conclusion: "The loss of formation of actinotrichia during evolution may have induced profound changes in the morphology of the adult pectoral fins that perhaps led to short appendages without lepidotrichia and to gene expression profiles conducive to polydactyly in the earliest tetrapod species. Thus, the loss of actinotrichia may have contributed to the evolutionary transition from fin to limb."


The team's next steps are to use alternative methods of gene silencing of and1 and and2 (remember that morpholinos are only transient silencers) to see whether the fin ray will develop and what it will look like (perhaps a limb with multiple digits?!).  The team may also introduce the gene into tetrapod species and see if they can cause fins in normally limbed animals.