Lifetime monogamy and the evolution of eusociality

All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton''s rule (br_s > r_oc), but implies that relatedness cancels out of the equation because average relatedness to siblings (r_s) and offspring (r_o) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton''s rule.     

The evolution of face processing in primates

The ability to recognize faces is an important socio-cognitive skill that is associated with a number of cognitive specializations in humans. While numerous studies have examined the presence of these specializations in non-human primates, species where face recognition would confer distinct advantages in social situations, results have been mixed. The majority of studies in chimpanzees support homologous face-processing mechanisms with humans, but results from monkey studies appear largely dependent on the type of testing methods used. Studies that employ passive viewing paradigms, like the visual paired comparison task, report evidence of similarities between monkeys and humans, but tasks that use more stringent, operant response tasks, like the matching-to-sample task, often report species differences. Moreover, the data suggest that monkeys may be less sensitive than chimpanzees and humans to the precise spacing of facial features, in addition to the surface-based cues reflected in those features, information that is critical for the representation of individual identity. The aim of this paper is to provide a comprehensive review of the available data from face-processing tasks in non-human primates with the goal of understanding the evolution of this complex cognitive skill.     

The relative rate of DNA evolution in primates

In 73 relative-rate tests involving the sequences of 17 genes between humans and six nonhuman primate taxa, there is only one significant (P less than 0.01) difference in evolutionary rate--i.e., that between human and Old World-monkey psi eta-globin genes. No evolutionary rate difference between humans and Old World monkeys is evident from analysis of 18 other genes with a total length of 6 kb. This and the comparison, between humans and other primate taxa, of new extended psi eta-globin sequences suggest that earlier observations of evolutionary-rate differences between humans and other primates were based on differences that are peculiar to psi eta-globin and that are not representative of the whole genome, which appears to be evolving at a stochastically uniform rate. This is supported by whole-genome single-copy DNA and mitochondrial DNA comparisons, neither of which shows any evidence of evolutionary-rate variation among primate taxa. Uniformity in the evolutionary rate of the DNA of primate and other mammalian taxa is inconsistent with current mammalian fossil-record interpretation. Either there has been a general slowing down in rate across lineages or the fossil record has been misinterpreted.     

The evolution of color vision in the primates

There will be no difficulty in seeing how and by what mixtures the colors are made … He, however, who should attempt to verify all this by experiment would forget the difference of the human and the divine nature. For God only has the knowledge and also the power which are able to combine many things into one and again resolve the one into many. But no man either is or ever will be able to accomplish either the one or the other operation.The law of proportion according to which the several colors are formed, even if a man knew he would be foolish in telling, for he could not give any necessary reason, nor indeed any tolerable or probable explanation of them (Jowett, 1871).     

Sexually transmitted infection and the evolution of serial monogamy

The selective forces shaping mating systems have long been of interest to biologists. One particular selective pressure that has received comparatively little attention is sexually transmitted infections (STIs). While it has been hypothesized that STIs could drive the evolutionary emergence of monogamy, there is little theoretical support. Here we use an evolutionary invasion analysis to determine what aspects of pathogen virulence and transmission are necessary for serial monogamy to evolve in a promiscuous population. We derive a biologically intuitive invasion condition in terms of population-specific quantities. From this condition, we obtain two main results. First, when pathogen virulence causes mortality rather than sterility, monogamy is more likely to evolve. Second, we find that at intermediate pathogen transmission rates, monogamy is the most selectively advantageous, whereas at high- and low-transmission rates, monogamy is generally selected against. As a result, it is possible for a pathogen to be highly virulent, yet for promiscuity to persist.     

Phylogeny and molecular evolution in primates

Statistical methods for estimating the branching order and the branching dates from DNA sequence data, taking into account of the rate variation among lineages, are reviewed. An application of the methods to data from primates suggests that chimpanzee is the closest relative of man, and further suggests that these two species diverged about 4-5 million years ago.     

Rates of molecular evolution of primates

This review considers the history and the current state of the debatable issue of variation in accumulation rates of mutational substitutions in the phylogeny of humans and other primates. Arguments pro and contra the hypothesis on gradually decreasing tempo of molecular evolution of humans and apes are discussed. It is shown that data on proteins and (nuclear and mitochondrial) DNA confirm this hypothesis. The conclusion is drawn that the total rate of mutation accumulation is determined by a number of interacting factors. The primary of these factors in most cases (including that of hominids) is generation time, which is closely associated with the number of germ cell divisions. At the same time, fixation rates of nonsynonymous substitutions are also affected by various forms of selection.     

Olfactory evolution and behavioral ecology in primates

Primates are usually thought of as "visual" mammals, and several comparative studies have emphasized the role of vision in primate neural and sociocognitive specialization. Here I explore the role of olfactory systems, using phylogenetic analysis of comparative volumetric data. The relative sizes of the main olfactory bulb (MOB) and accessory olfactory bulb (AOB) tend to show different evolutionary patterns in accordance with their different functions. Although there is some evidence of correlated evolution of the two systems, this is apparent in only one clade (the strepsirhines). As predicted, the MOBs correlate predominantly with ecological factors (activity period and diet), while the AOBs correlate with social and mating systems. Related olfactory structures (i.e., the piriform cortex and amygdala) exhibit correlated evolution with the AOBs but not with the MOBs, and the corticobasolateral part of the amygdala exhibits a correlation with social group size in platyrrhines similar to that observed for the AOB. These social system correlations support the idea that there is an olfactory dimension to the concept of the social brain.     

Convergent evolution in primates and an insectivore

The cardiovascular risk factor LPA has a puzzling distribution among mammals, its presence being limited to a subset of primates and a member of the insectivore lineage, the hedgehog. To explore the evolutionary history of LPA, we performed extensive genomic sequence comparisons of multiple species with and without an LPA gene product, such as human, baboon, hedgehog, lemur, and mouse. This analysis indicated that LPA arose independently in a subset of primates, including baboon and human, and an insectivore, the hedgehog, and was not simply lost by species lacking it. The similar structural domains shared by the hedgehog and primate LPA indicate that they were formed by a unique molecular mechanism involving the convergent evolution of paralogous genes in these distant species.     

The evolution of the cortico-cerebellar complex in primates: anatomical connections predict patterns of correlated evolution

Investigations into the evolution of the primate brain have tended to neglect the role of connectivity in determining which brain structures have changed in size, focusing instead on changes in the size of the whole brain or of individual brain structures, such as the neocortex, in isolation. We show that the primate cerebellum, neocortex, vestibular nuclei and relays between them exhibit correlated volumetric evolution, even after removing the effects of change in other structures. The patterns of correlated evolution among individual nuclei correspond to their known patterns of connectivity. These results support the idea that the brain evolved by mosaic size change in arrays of functionally connected structures. Furthermore, they suggest that the much discussed expansion of the primate neocortex should be re-evaluated in the light of conjoint cerebellar expansion.     

Molecular evolution of aerobic energy metabolism in primates

As part of our goal to reconstruct human evolution at the DNA level, we have been examining changes in the biochemical machinery for aerobic energy metabolism. We find that protein subunits of two of the electron transfer complexes, complex III and complex IV, and cytochrome c, the protein carrier that connects them, have all undergone a period of rapid protein evolution in the anthropoid lineage that ultimately led to humans. Indeed, subunit IV of cytochrome c oxidase (COX; complex IV) provides one of the best examples of positively selected changes of any protein studied. The rate of subunit IV evolution accelerated in our catarrhine ancestors in the period between 40 to 18 million years ago and then decelerated in the descendant hominid lineages, a pattern of rate changes indicative of positive selection of adaptive changes followed by purifying selection acting against further changes. Besides clear evidence that adaptive evolution occurred for cytochrome c and subunits of complexes III (e.g., cytochrome c(1)) and IV (e.g., COX2 and COX4), modest rate accelerations in the lineage that led to humans are seen for other subunits of both complexes. In addition the contractile muscle-specific isoform of COX subunit VIII became a pseudogene in an anthropoid ancestor of humans but appears to be a functional gene in the nonanthropoid primates. These changes in the aerobic energy complexes coincide with the expansion of the energy-dependent neocortex during the emergence of the higher primates. Discovering the biochemical adaptations suggested by molecular evolutionary analysis will be an exciting challenge.     

Molecular evolution of immunoglobulin superfamily genes in primates

Genes of the immunoglobulin superfamily (IgSF) have a wide variety of cellular activities. In this study, we investigated molecular evolution of IgSF genes in primates by comparing orthologous sequences of 249 IgSF genes among human, chimpanzee, orangutan, rhesus macaque, and common marmoset. To evaluate the non-synonymous/synonymous substitution ratio (ω), we applied Bn-Bs program and PAML program. IgSF genes were classified into 11 functional categories based on the Gene Ontology (GO) database. Among them, IgSF genes in three functional categories, immune system process (GO:0002376), defense response (GO:0006952), and multi-organism process (GO:0051704), which are tightly linked to the regulation of immune system had much higher values of ω than genes in the other GO categories. In addition, we estimated the average values of ω for each primate lineage. Although each primate lineage had comparable average values of ω, the human lineage showed the lowest ω value for the immune-related genes. Furthermore, 11 IgSF genes, SIGLEC5, SLAMF6, CD33, CD3E, CEACAM8, CD3G, FCER1A, CD48, CD4, TIM4, and FCGR2A, were implied to have been under positive selective pressure during the course of primate evolution. Further sequence analyses of CD3E and CD3G from 23 primate species suggested that the Ig domains of CD3E and CD3G underwent the positive Darwinian selection.     

Visual specialization and brain evolution in primates.

Several theories have been proposed to explain the evolution of species differences in brain size, but no consensus has emerged. One unresolved question is whether brain size differences are a result of neural specializations or of biological constraints affecting the whole brain. Here I show that, among primates, brain size variation is associated with visual specialization. Primates with large brains for their body size have relatively expanded visual brain areas, including the primary visual cortex and lateral geniculate nucleus. Within the visual system, it is, in particular, one functionally specialized pathway upon which selection has acted: evolutionary changes in the number of neurons in parvocellular, but not magnocellular, layers of the lateral geniculate nucleus are correlated with changes in both brain size and ecological variables (diet and social group size). Given the known functions of the parvocellular pathway, these results suggest that the relatively large brains of frugivorous species are products of selection on the ability to perceive and select fruits using specific visual cues such as colour. The separate correlation between group size and visual brain evolution, on the other hand, may indicate the visual basis of social information processing in the primate brain.     

Constraints on masticatory system evolution in anthropoid primates

It is well established that some observed patterns of force production in the primate masticatory system match those predicted by a simplified lever model. This model is also commonly invoked in adaptive explanations of craniodental diversity. However, systematic studies of the predictive power of this model are missing, leaving open the possibility that factors not traditionally included in the model alter the function and evolution of the masticatory system. One such factor was proposed for mammals generally by Greaves ([1978] J. Zool. (Lond.) 184:271-285), who argued that the temporomandibular joint (TMJ) was poorly suited to being pulled apart. In this constrained lever model, the avoidance of joint distraction leads to limitations on masticatory system form and function. The goal of the present study was to quantify masticatory system diversity in anthropoid primates for comparison with these predictions. Results indicate that all sampled taxa exhibit a form that is consistent with selection against regular distraction of the TMJ. Also apparent from observed patterns of scaling is a regular interaction among a limited set of cranial and dental dimensions, in accordance with the constrained model. However, the data indicate that specific positional relationships among the muscles, joints, and teeth differ from those predicted by Greaves (1978). The pattern of deviation suggests that selection has favored a conservative masticatory system configuration that safeguards the TMJ from distraction during the dynamic processing of irregular foods. The resulting buffered model leads to alternative hypotheses regarding the response of the masticatory system to dietary selection pressures. It may, therefore, improve our understanding of the adaptive significance of primate craniofacial form.     

Language evolution: the origin of meaning in primates

Research on alarm calls has yielded rare glimpses into the minds of our closest relatives. A new study suggests that primates monitor the effect alarm calls have on others.     

Adaptive evolution of the IgA hinge region in primates

IgA is a major component that prevents the penetration of pathogenic bacteria into mucosal surfaces. The IgA antibody is cleaved at the IgA hinge region with high specificity by IgA-specific proteases produced by several pathogenic bacteria. We conducted a genomic sequence analysis of the IgA genes of a wide spectrum of primates, including the first intron and second exon, which consist of the hinge region and the CH2 domain, to find evidence of positive selection. Because the hinge region is quite small, we combined the largest collection of sequences that could be clearly aligned and evaluated the total numbers of synonymous and nonsynonymous substitutions on the phylogenetic tree. The nonsynonymous to synonymous substitution ratio (d(N)/d(S) test) showed that hominoids, Old World monkeys, and New World monkeys have d(N)/d(S) ratios of 5.4, 6.3, and 4.2, respectively. Fisher's exact probability tests showed statistical significance for the Old World monkey. Because the substitution rates of the flanking sequences are more or less similar to the synonymous rates of the hinge region, these high values of d(N)/d(S) should be the result of positive selection at the hinge region. Combining the high sequence variability in each population and the highly accelerated nonsynonymous substitution rates in the hinge region, we conclude that this unusual IgA evolution is a molecular evidence of adaptive evolution possibly caused by the host-parasite relationship.