Evolution of snake venom disintegrins by positive Darwinian selection

PII-disintegrins, cysteine-rich polypeptides broadly distributed in the venoms of geographically diverse species of vipers and rattlesnakes, antagonize the adhesive functions of beta(1) and beta(3) integrin receptors. PII-disintegrins evolved in Viperidae by neofunctionalization of disintegrin-like domains of duplicated PIII-snake venom hemorrhagic metalloproteinase (SVMP) genes recruited into the venom proteome before the radiation of the advanced snakes. Minimization of the gene (loss of introns and coding regions) and the protein structures (successive loss of disulfide bonds) underpins the postduplication divergence of disintegrins. However, little is known about the underlying genetic mechanisms that have generated the structural and functional diversity among disintegrins. Phylogenetic inference and maximum likelihood-based codon substitution approaches were used to analyze the evolution of the disintegrin family. The topology of the phylogenetic tree does not parallel that of the species tree. This incongruence is consistent with that expected for a multigene family undergoing a birth-and-death process in which the appearance and disappearance of loci are being driven by selection. Cysteine and buried residues appear to be under strong purifying selection due to their role in maintaining the active conformation of disintegrins. Divergence of disintegrins is strongly influenced by positive Darwinian selection causing accelerated rate of substitution in a substantial proportion of surface-exposed disintegrin residues. Global and lineage-specific sites evolving under diversifying selection were identified. Several sites are located within the integrin-binding loop and the C-terminal tail, two regions that form a conformational functional epitope. Arginine-glycine-aspartic acid (RGD) was inferred to represent the ancestral integrin-recognition motif, which emerged from the subgroup of PIII-SVMPs bearing the RDECD sequence. The most parsimonious nucleotide substitution model required for the emergence of all known disintegrin's integrin inhibitory motifs from an ancestral RGD sequence involves a minimum of three mutations. The adaptive advantage of the emergence of motifs targeting beta(1) integrins and the role of positively selected sites located within nonfunctional disintegrin regions appear to be difficult to rationalize in the context of a predator-prey arms race. Perhaps, this represents a consequence of the neofunctionalization potential of the disintegrin domain, a feature that may underlie its recruitment into the venom proteome followed by its successful transformation into a toxin.     

Evolution of adaptive phenotypic traits without positive Darwinian selection

Recent evidence suggests the frequent occurrence of a simple non-Darwinian (but non-Lamarckian) model for the evolution of adaptive phenotypic traits, here entitled the plasticity-relaxation-mutation (PRM) mechanism. This mechanism involves ancestral phenotypic plasticity followed by specialization in one alternative environment and thus the permanent expression of one alternative phenotype. Once this specialization occurs, purifying selection on the molecular basis of other phenotypes is relaxed. Finally, mutations that permanently eliminate the pathways leading to alternative phenotypes can be fixed by genetic drift. Although the generality of the PRM mechanism is at present unknown, I discuss evidence for its widespread occurrence, including the prevalence of exaptations in evolution, evidence that phenotypic plasticity has preceded adaptation in a number of taxa and evidence that adaptive traits have resulted from loss of alternative developmental pathways. The PRM mechanism can easily explain cases of explosive adaptive radiation, as well as recently reported cases of apparent adaptive evolution over ecological time.     

The Evolution of Evolutionary Thinking in Chile

The scientific study of evolution in Chile has experienced periods of diversification and stasis, depending upon the social and political context at different times. In the eighteenth century, most of the natural history research consisted of systematics and taxonomy and, as in most of South America, this task was performed mainly by natural historian theologists. Later, the immigration of European scientists to Chile after independence from Spain in 1810 improved substantially its knowledge of the local biota and stimulated the diversification of naturalists in the country. Research in modern biology and the teaching of genetics in Chile can be traced back to Giovanni Noe, an Italian zoologist who had a profound impact in the first third of the twentieth century. In the 1960s–70s, Danko Brncic, a population geneticist educated in the tradition of Dobzhansky and the modern synthesis, led the most important diversification process in the study of evolutionary biology in the country. However, the military coup in 1973 brought this radiation to a sudden stop and produced a stasis period associated with the subsequent 17-year dictatorship. Evolutionary biology recovered its status after the re-establishment of democracy, and it is currently experiencing an exciting and renewed diversification period that has led to the foundation of the Chilean Society of Evolutionary Biology, the only scientific society for the study of evolution in Latin America. One of the missions of the Society is to bridge the gap between scientists and science educators in order to improve the teaching of evolution at different levels both in secular and religious schools. Even though the Roman Catholic Church has been a pivotal institution in the development of Chilean society, debate on evolutionism—creationism issues has been largely absent both in public and academic discussions. The influence of religion on science education has been sporadic, and mostly related to omission rather than tergiversation of scientific information in biology textbooks. Currently, schools are obliged by law to teach the basics of evolution in K-12 and K-16 levels (or their local equivalents). Because of this, there is little at present that suggests an organized creationist or intelligent design movement surge in the near future. Nevertheless, the high percentage of religiosity in Chile, together with the observation that the moral values of Chilean society are among the most conservative in the world, provide good reasons to remain vigilant.     

Unfinished Stories on Viral Quasispecies and Darwinian Views of Evolution

Experimental evidence that RNA virus populations consist of distributions of mutant genomes, termed quasispecies, was first published 31 years ago. This work provided the earliest experimental support for a theory to explain a system that replicated with limited fidelity and to understand the self-organization and adaptability of early life forms on Earth. High mutation rates and quasispecies dynamics of RNA viruses are intimately related to both viral disease and antiviral treatment strategies. Moreover, the quasispecies concept is being applied to other biological systems such as cancer research in which cellular mutant spectra can be also detected. This review addresses some of the unanswered questions regarding viral and theoretical quasispecies concepts as well as more practical aspects concerning resistance to antiviral treatments and pathogenesis.     

The dawn of Darwinian medicine

While evolution by natural selection has long been a foundation for biomedical science, it has recently gained new power to explain many aspects of disease. This progress results largely from the disciplined application of what has been called the adaptations program. We show that this increasingly significant research paradigm can predict otherwise unsuspected facets of human biology, and that it provides new insights into the causes of medical disorders, such as those discussed below: 1. Infection. Signs and symptoms of the host-parasite contest can be categorized according to whether they represent adaptations or costs for host or parasite. Some host adaptations may have contributed to fitness in the Stone Age but are obsolete today. Others, such as fever and iron sequestration, have been incorrectly considered harmful. Pathogens, with their large populations and many generations in a single host, can evolve very rapidly. Acquisition of resistance to antibiotics is one example. Another is the recently demonstrated tendency to change virulence levels in predictable ways in response to changed conditions imposed incidentally by human activities. 2. Injuries and toxins. Mechanical injuries or stressful wear and tear are conceptually simpler than infectious diseases because they are not contests between conflicting interests. Plant-herbivore contests may often underlie chemical injury from the defensive secondary compounds of plant tissues. Nausea in pregnancy, and allergy, may be adaptations against such toxins. 3. Genetic factors. Common genetic diseases often result from genes maintained by other beneficial effects in historically normal environments. The diseases of aging are especially likely to be associated with early benefits. 4. Abnormal environments. Human biology is designed for Stone Age conditions. Modern environments may cause many diseases-for example, deficiency syndromes such as scurvy and rickets, the effects of excess consumption of normally scarce nutrients such as fat and salt, developmental diseases such as myopia, and psychological reactions to novel environments. The substantial benefits of evolutionary studies of disease will be realized only if they become central to medical curricula, an advance that may at first require the establishment of one or more research centers dedicated to the further development of Darwinian medicine.     

Rapid Evolution by Positive Darwinian Selection in T-Cell Antigen CD4 in Primates

CD4, an integral membrane glycoprotein, plays a critical role in the immune response and in the life cycle of simian and human immunodeficiency virus (SIV and HIV). Pairwise comparisons of orthologous human and mouse genes show that CD4 is evolving much faster than the majority of mammalian genes. The acceleration is too great to be attributed to a simple relaxation of the action of purifying selection alone. Here we show that the selective pressure acting on CD4 is highly variable between regions in the protein and identify codon sites under strong positive selection. We reconstruct the coding sequences for ancestral primate CD4s and model tertiary structures of all ancestral and extant sequences. Structural mapping of positively selected sites shows they distribute on the surface of the D1 domain of CD4, where the exogenous SIV gp120 protein binds. Moreover, structural models of the ancestral sequences show substantially larger variation in the interfacial electrostatic charge on CD4 and in the surface complementary between CD4 and gp120 in CD4 lineages from primates with natural SIV infections than those without. Thus, positive selection on CD4 among primates may reflect forces driven by SIV infection and could provide a link between changes in sequence and structure of CD4 during evolution and the interaction with the immunodeficiency virus.     

The Role of Ontogeny in the Evolution of Human Cooperation

To explain the evolutionary emergence of uniquely human skills and motivations for cooperation, Tomasello et al. (2012, in Current Anthropology 53(6):673–92) proposed the interdependence hypothesis. The key adaptive context in this account was the obligate collaborative foraging of early human adults. Hawkes (2014, in Human Nature 25(1):28–48), following Hrdy (Mothers and Others, Harvard University Press, 2009), provided an alternative account for the emergence of uniquely human cooperative skills in which the key was early human infants’ attempts to solicit care and attention from adults in a cooperative breeding context. Here we attempt to reconcile these two accounts. Our composite account accepts Hrdy’s and Hawkes’s contention that the extremely early emergence of human infants’ cooperative skills suggests an important role for cooperative breeding as adaptive context, perhaps in early Homo. But our account also insists that human cooperation goes well beyond these nascent skills to include such things as the communicative and cultural conventions, norms, and institutions created by later Homo and early modern humans to deal with adult problems of social coordination. As part of this account we hypothesize how each of the main stages of human ontogeny (infancy, childhood, adolescence) was transformed during evolution both by infants’ cooperative skills “migrating up” in age and by adults’ cooperative skills “migrating down” in age.     

Thinking About the Evolution of Photosynthesis

Photosynthesis is an ancient process on Earth. Chemical evidence and recent fossil finds indicate that cyanobacteria existed 2.5-2.6 billion years (Ga) ago, and these were certainly preceded by a variety of forms of anoxygenic photosynthetic bacteria. Carbon isotope data suggest autotrophic carbon fixation was taking place at least a billion years earlier. However, the nature of the earliest photosynthetic organisms is not well understood. The major elements of the photosynthetic apparatus are the reaction centers, antenna complexes, electron transfer complexes and carbon fixation machinery. These parts almost certainly have not had the same evolutionary history in all organisms, so that the photosynthetic apparatus is best viewed as a mosaic made up of a number of substructures each with its own unique evolutionary history. There are two schools of thought concerning the origin of reaction centers and photosynthesis. One school pictures the evolution of reaction centers beginning in the prebiotic phase while the other school sees reaction centers evolving later from cytochrome b in bacteria. Two models have been put forth for the subsequent evolution of reaction centers in proteobacteria, green filamentous (non-sulfur) bacteria, cyanobacteria, heliobacteria and green sulfur bacteria. In the selective loss model the most recent common ancestor of all subsequent photosynthetic systems is postulated to have contained both RC1 and RC2. The evolution of reaction centers in proteobacteria and green filamentous bacteria resulted from the loss of RC1, while the evolution of reaction centers in heliobacteria and green sulfur bacteria resulted from the loss of RC2. Both RC1 and RC2 were retained in the cyanobacteria. In the fusion model the most recent common ancestor is postulated to have given rise to two lines, one containing RC1 and the other containing RC2. The RC1 line gave rise to the reaction centers of heliobacteria and green sulfur bacteria, and the RC2 line led to the reaction centers of proteobacteria and green filamentous bacteria. The two reaction centers of cyanobacteria were the result of a genetic fusion of an organism containing RC1 and an organism containing RC2. The evolutionary histories of the various classes of antenna/light-harvesting complexes appear to be completely independent. The transition from anoxygenic to oxygenic photosynthesis took place when the cyanobacteria learned how to use water as an electron donor for carbon dioxide reduction. Before that time hydrogen peroxide may have served as a transitional donor, and before that, ferrous iron may have been the original source of reducing power.     

The Role of Off-line Communication in Human Evolution

The existence of embodied communication in humans places them among other living systems and helps to differentiate sign patterns that are common to all bioforms from those that are peculiarly human. Despite the fact that the biological roots of communication have been proven, the understanding of human forms of discourse is still far from being clarified. The main question remains: when and why did humans acquire the ability to exchange messages via speech? My thesis is that it became possible only after humans made a shift from on-line to off-line interaction and learned to communicate in the interpersonal mode via externalized analog codes that constitute the various forms of human culture.     

Finalism in Darwinian and Lamarckian Evolution: Lessons from Epigenetics and Developmental Biology

Finalist (teleological) implications have been described for both Darwinian and Lamarckian theories, even though finalism appears to be more commonly associated with Lamarckism. Biologists have focused on finding final causes to explain evolutionary novelties through, for example, applying the ??what for??? question to address experimental observations. Now epigenetics, together with developmental biology, may allow us to focus on the efficient causes leading to evolutionary change, asking the ??how??? question, considering environmental influences as inducers of genomic change. This is a whole under-studied dimension in evolutionary studies. In this paper, I discuss how epigenetics and developmental biology can help integrate two important ways in which the environment affects evolution: through inducing or through restricting the emergence of new phenotypes. I also discuss which aspects of both theories should be reconsidered in the face of current knowledge in epigenetics and where the emphasis of evolutionary experiments should be placed. Important goals of evolution related epigenetic studies should be: (i) to experimentally consider the separation among the origin of characters in a lineage and its further fixation, in order to address these processes in a proper dimension, (ii) to build the cause-effect relation between the factors inducing epigenetic changes and consequent changes in population parameters, and (iii) to consider that the arising of new characters is modulated by physiological and developmental constraints, and that this process is not related to a purpose or focused to solve an ecological, physiological or evolutionary challenge.     

The Haeckelian hijack of Darwinian deism

ABSTRACT

Ernst Haeckel (1834–1919) is most recalled in the history of biology for his Recapitulation Theory and the allegedly fudged illustrations of embryos that he presented in support of that case. Less well known is his contribution to abiogenesis theory, which he incorporated into evolutionary theory. In so doing, Haeckel, a vitriolic atheist, was instrumental in inserting atheism into the evolutionary mindset. While anti-evolution propaganda commonly makes Darwin out to be the villain of the piece, the association of evolution in the broad sense of the word with atheism arises more from the Haeckelian legacy than from Darwin’s initially conciliatory deism or Huxley’s non-committal agnosticism.