Bioenergetic Constraints on the Evolution of Complex Life

All morphologically complex life on Earth, beyond the level of cyanobacteria, is eukaryotic. All eukaryotes share a common ancestor that was already a complex cell. Despite their biochemical virtuosity, prokaryotes show little tendency to evolve eukaryotic traits or large genomes. Here I argue that prokaryotes are constrained by their membrane bioenergetics, for fundamental reasons relating to the origin of life. Eukaryotes arose in a rare endosymbiosis between two prokaryotes, which broke the energetic constraints on prokaryotes and gave rise to mitochondria. Loss of almost all mitochondrial genes produced an extreme genomic asymmetry, in which tiny mitochondrial genomes support, energetically, a massive nuclear genome, giving eukaryotes three to five orders of magnitude more energy per gene than prokaryotes. The requirement for endosymbiosis radically altered selection on eukaryotes, potentially explaining the evolution of unique traits, including the nucleus, sex, two sexes, speciation, and aging.Evolutionary theory has enormous explanatory power and is understood in detail at the molecular genetic level, yet it cannot easily predict even the past. The history of life on Earth is troubling. Life apparently arose very early, perhaps 4 billion years ago, but then remained essentially bacterial for probably some 2–3 billion years. Bacteria and archaea explored almost every conceivable metabolic niche and still dominate in terms of biomass. Yet, in morphological diversity and genomic complexity, bacteria barely begin to compare with eukaryotes, even at the level of cells, let alone multicellular plants and animals. Eukaryotes are monophyletic and share a common ancestor that by definition arose only once, probably between 1.5 and 2 billion years ago, although the dates are poorly constrained (Knoll et al. 2006; Parfrey et al. 2011). The eukaryotic common ancestor already had a nucleus, nuclear pore complexes, introns and exons, straight chromosomes, mitosis and meiotic sex, a dynamic cytoskeleton, an endoplasmic reticulum, and mitochondria, making it difficult to trace the evolution of these traits from a prokaryotic state (Koonin 2010). The “eukaryotic niche”—limited metabolic diversity but enormous morphological complexity—was never invaded by prokaryotes. In short, life arose early, stagnated in morphological complexity for several billion years, and then rather abruptly gave rise to a single group—the eukaryotes—which explored the morphological realm of life in ways never seen in bacteria or archaea.Consider the possibility of life evolving on other planets. Would it follow a similar trajectory? If not, why not? Evolutionary theory gives little insight. The perplexing history of life on Earth conceals a paradox relating to natural selection. If basal eukaryotic traits such as the nucleus, meiotic sex, and phagocytosis arose by selection, starting with a prokaryotic ancestor, and each step offered some small advantage over the last, then why don’t the same traits arise repeatedly in prokaryotes too? Prokaryotes made many a start. There are examples of bacteria or archaea with nucleus-like structures (Lindsay et al. 2001), recombination (Smith et al. 1993), linear chromosomes (Bentley et al. 2002), internal membranes (Pinevich 1997), multiple replicons (Robinson and Bell 2007), giant size (Schulz and Jorgensen 2001), extreme polyploidy (Mendell et al. 2008), a dynamic cytoskeleton (Vats and Rothfield 2009), predation (Davidov and Jurkevitch 2009), parasitism (Moran 2007), introns and exons (Simon and Zimmerly 2008), intercellular signaling (Waters and Bassler 2005), endocytosis-like processes (Lonhienne et al. 2010), and even endosymbionts (Wujek 1979; von Dohlen et al. 2001). Yet, for each of these traits, bacteria and archaea stopped well short of the baroque complexity of eukaryotes. Compare this with the evolution of eyes. From a simple, light-sensitive spot in an early metazoan, morphologically disparate eyes arose on scores of occasions (Vopalensky and Kozmic 2009). This is exactly what evolutionary theory predicts. Each step offers an advantage in its own ecological setting, so morphologically different eyes arise on multiple occasions. Why is this not the case for traits such as the nucleus, meiotic sex, and phagocytosis? To suggest that lateral gene transfer (LGT) or bacterial conjugation is equivalent to meiotic sex will not do: Neither involves a systematic and reciprocal exchange of alleles across the entire genome.The simplest explanation is a bottleneck. The “big bang” radiation of major eukaryotic supergroups, combined with the apparent absence of surviving evolutionary intermediates between prokaryotes and the last eukaryotic common ancestor, does indeed hint at a bottleneck at the origin of eukaryotes. There is no shortage of environmental possibilities, from snowball glaciations to rising atmospheric oxygen. The most widely held explanation contends that when oxygen levels rose after the great oxidation event, some proto-eukaryotic cells acquired mitochondria, which protected them against oxygen toxicity (Andersson and Kurland 1999) and enabled them to exploit oxygen as a terminal electron acceptor in respiration (Sagan 1967), giving the first eukaryotes an enormous competitive advantage. They swiftly occupied new niches made available by oxygen, outcompeting to extinction any other prokaryotes that tried subsequently to invade this niche (de Duve 2007; Gross and Bhattacharya 2010). But this is an evolutionary “just-so story” and has no evidence to support it. The idea that mitochondria might protect against oxygen toxicity is nonsense: The single-electron donors of respiratory chains are among the most potent free-radical generators known. And what was to stop facultatively aerobic bacteria—from which the mitochondria evolved, hence already present—from occupying the aerobic niche first?In fact, the limited evidence available suggests that oxygen had little to do with it (Müller et al. 2012; van der Giezen and Lenton 2012). A large, diverse group of morphologically simple protists dubbed archezoa are the key here. The archezoa appear to lack mitochondria; and three decades ago, looked to branch deeply in the eukaryotic tree. Cavalier-Smith postulated that some archezoa might be primitively amitochondriate: surviving evolutionary intermediates between prokaryotes and eukaryotes (Cavalier-Smith 1987, 1989). But 20 years of careful molecular biology and phylogenetics have shown that all known archezoa possess specialized organelles that derive from mitochondria, namely hydrogenosomes or mitosomes (Keeling 1998; Embley and Martin 2006; van der Giezen 2009; Archibald 2011). The archezoa are obviously not real evolutionary intermediates, and radical developments in phylogenomics have transformed the eukaryotic tree to a “big-bang” radiation with no early branching archezoa (Koonin 2010). The archezoa remain significant not because they are genuine evolutionary intermediates, but because they are true ecological intermediates. Critically, they were not outcompeted to extinction by more sophisticated aerobic eukaryotes. On the contrary, they lost their capacity for aerobic respiration and depend instead on anaerobic fermentations, yet remain, morphologically, more complex than bacteria or archaea.The fact that the archezoa are a phylogenetically disparate group that arose on multiple occasions is equally significant. The “intermediate” niche is viable and was invaded many times, without the new arrivals being outcompeted to extinction by existing cells, or vice versa. Yet each time the invader was an anaerobic eukaryote, which adapted by reductive evolution to the niche—not bacteria or archaea evolving slightly greater complexity. What is the likelihood of this bias? Given at least 20 independent origins of archezoa (van der Giezen 2009; Müller et al. 2012), the probability of these ecological intermediates arising each time from the eukaryotes rather than prokaryotes is less than one in a million. It is far more parsimonious to assume that there was something about the structure of eukaryotes that facilitated their invasion of this intermediate niche; and, conversely, something about the structure of prokaryotes that tended to preclude their evolution of greater morphological complexity. But this quite reasonable statement is loaded because it implies that prokaryotes existed for nearly 4 billion years, and throughout that time showed no tendency to evolve greater morphological complexity. In stark contrast, eukaryotes arose just once, a seemingly improbable event.Here I argue that the constraint on prokaryotes was bioenergetic. There was, indeed, a bottleneck at the origin of eukaryotes, but it was biological (restrictive), not environmental (selective). It related to the physical structure of prokaryotic cells: Both bacteria and archaea respire across their plasma membrane. I make three key points, which arguably apply to life elsewhere in the universe, and are therefore proposed as biological principles that could guide our understanding of life generally: (1) chemiosmotic coupling is as universal as the genetic code, for fundamental reasons relating to the origin of life; (2) prokaryotes are constrained by chemiosmotic coupling across their plasma membrane, but eukaryotes escaped this constraint through a rare and stochastic endosymbiosis between two prokaryotes, giving them orders of magnitude more energy per gene; and (3) this endosymbiosis, in turn, produced a unique genomic asymmetry, transforming the selection pressures acting on eukaryotes and driving the evolution of unique eukaryotic traits.     

Life History Consequences of Bioenergetic and Biomechanical Constraints on Migration

In this paper I test the hypothesis that bioenergetic and biomechanicalconstraints to migration play a pivotal role in shaping thelife history characteristics of migrants. Firstly, I examinebioenergetic constraints on the ability to migrate by activetransport and how they shape the life histories of insects andfish, and, secondly, the consequences of biomechanical constraintsto the migration by passive transport in insects and spiders. In both insects and fish the mass-specific energetic costs ofactive transport (flight and swimming, respectively) decreasewith body size, and hence selection should favor large sizein migrant species. Because their habitats are ephemeral, migrantinsects must grow rapidly. In fish, migrant species are ableto exploit resources unavailable to more sedentary species andhence should also show an enhanced rate of growth. These predictionsare supported by comparisons within populations, between populations,and among species in both groups. In contrast to the above, biomechanical factors limit the uppersize at which insects and spiders can migrate by passive transport.Theory predicts that ballooning will be most likely in spidersconsiderably less than 6 mm in length. Therefore, species thatmigrate as adults are predicted to be smaller than those thatdo not. This prediction is supported by a comparison of migratoryand non-migratory spider species from the United Kingdom. Theaverage length of species that migrate as adults, and of migratingyoung of spiders too large to balloon as adults, is about 2mm. Further, within this geographic species assemblage, thesize distribution of adult spiders is markedly peaked in the2 mm region, suggesting that biomechanical constraints on ballooningmay have a major influence on the evolution of body size inspiders.     

Bioenergetic Constraints on Microbial Hydrogen Utilization in Precambrian Deep Crustal Fracture Fluids

Precambrian Shield rocks host the oldest fracture fluids on Earth, with residence times up to a billion years or more. Water–rock reactions in these fracture systems over geological time have produced highly saline fluids, which can contain millimolar concentrations of H₂. Mixing of these ancient Precambrian fluids with meteoric or palaeo-meteoric water can occur through tectonic fracturing, providing microbial inocula and redox couples to fuel blooms of subsurface growth. Here, we present geochemical and microbiological data from a series of borehole fluids of varying ionic strength (0.6–6.4 M) from the Thompson Mine (Manitoba) within the Canadian Precambrian Shield. Thermodynamic calculations demonstrate sufficient energy for H₂-based catabolic reactions across the entire range of ionic strengths during mixing of high ionic strength fracture fluids with meteoric water, although microbial H₂ consumption and cultivable H₂-utilizing microbes were only detected in fluids of ≤1.9 M ionic strength. This pattern of microbial H₂ utilization can be explained by the higher potential bioenergetic cost of organic osmolyte synthesis at increasing ionic strengths. We propose that further research into the bioenergetics of osmolyte regulation in halophiles is warranted to better constrain the habitability zones of hydrogenotrophic ecosystems in both terrestrial subsurface, including potential future radioactive waste disposal sites, and other planetary body crustal environments, including Mars.     

Primate Group Size and Abundance in the Caatinga Dry Forest, Northeastern Brazil

The Caatinga dry forest poses a series of ecological challenges for mammals in general and primates in particular. The erratic rainfall pattern impacts on plant diversity and phenological patterns; from year to year there is marked variability in fruit production and failure to fruit is common. The harshness apparently accounts for the impoverished mammalian fauna. However, data on primate abundance, distribution, and possible environmental effects on primate density are lacking in this type of dry forest. I censused the primate community in 3 habitats of the Serra da Capivara National Park, Piaui, NE Brazil, over a total distance of 318 km. Overall, the abundance of primates in the Caatinga dry forest is very low as a consequence of low abundance of food resources both in space and time. Alouatta caraya (predominantly folivorous) occurs at extremely low density, and during the dry season are apparently confined to canyon areas, where trees retain their leaves. Callithrix jacchus has morphological feeding specializations for gum-eating, and gum is an important resource during food bottleneck periods. Nonetheless, Callithrix jacchus occurs at comparatively low densities. Group sizes for howlers and marmosets in the Caatinga are significantly smaller than in other forest types. Contrarily, Cebus apella libidinosus had an average group size within the range reported for Amazonian and Atlantic forests. Researchers consider the generalized diet of capuchins as the explanation for their similar abundance in different habitats, indicating relative independence from ecological constraints. However, I suggest that capuchin foraging style and cognitive abilities are important factors accounting for their unreduced group size and density even under extreme conditions.     

Low Primate Diversity and Abundance in Northern Amazonia and its Implications for Conservation

Large areas of the Rio Negro basin in Amazonia are covered by continuous tracts of tropical forest, but have few primate species. This is anomalous considering the general relationship between area and number of species. One possibility is that much of the forest is unsuitable habitat for most primates and the area of suitable habitat is much less than the forested area. This has important consequences for the design of reserves and predictions of the consequences of climate change, which tend to be based on broad categories based on satellite images, and not on information of species distributions within those broad categories. The study was conducted through diurnal and nocturnal line‐transect surveys in the Biodiversity Research Program 25‐km² permanent grid in Viruá National Park, which has vegetation associations typical of much of northern Amazonia. The highest primate diversity and abundances occurred in tall terra firme forests (58%), whereas inundated forests and scrublands, which cover 42 percent of the survey grid and 90.8 percent of the Viruá National Park, have virtually no primates. This suggests that parks and reserves in northwestern Amazonia will have to be very large to maintain viable populations of most primates and their ecological interactions, and that very broad habitat categories are not sufficient to make predictions about actual and future suitability of areas for primate conservation.     

Quantifying Primate Food Distribution and Abundance for Socioecological Studies: An Objective Consumer-centered Method

Food abundance and distribution have played a central role in the conceptual theory of primate socioecology. This theory predicts that agonistic (contest) competition should occur when food is distributed in discrete, defensible patches; in contrast, when food sources are distributed uniformly or randomly, nonagonistic (scramble) competition is expected. Primatologists usually measure resource density and patchiness from a botanical perspective, without an explicit link to the biology of the animal being studied. Such an approach may be irrelevant to how the animals view the dispersion of resources. For studies related to feeding competition, we suggest the use of a method that provides a consumer-based index of food distribution. We then describe such an approach and apply it to understand agonistic behavior in white-faced capuchins (Cebus capucinus), at Lomas Barbudal. Instead of choosing sample plots at random, we use each actual feeding tree of a group as the center of a sample plot and we use the monkey species’ average group spread as the sampling area. This focal tree method allows us to evaluate the resource availability both within and outside of the feeding tree during a particular feeding bout. To summarize the spatial distribution of food at the level of a foraging group, we define and use an extension of Lloyd’s Dispersion Index, Lloyd’s Extended Index (LEI), designed to allow the inclusion of resources of diverse sizes and species in a single measure. We evaluate if LEI can be used to predict the frequency of aggression, if changing the area of the plot alters these results, and if calculating LEI based on fruit abundance or fruit biomass better predicts the frequency of aggression in this population of capuchins. In support of socioecological predictions, our results show that the frequency of agonism in a focal tree declines as LEI increases. This relationship is significant when LEI is calculated using a 20-m plot size and weighting tree size by fruit counts, but not when using larger plot sizes, unweighted tree counts, or weighting by fruit biomass. Our approach demonstrates the importance of carefully considering plot size and different measures of food availability when testing socioecological models relating resource distribution and quality to aggression in nonhuman primates.     

Distribution and Abundance of the World's Smallest Primate,Microcebus berthae,in Central Western Madagascar

The distribution of most recently discovered or described lemur species remains poorly known, but many appear to have small geographical ranges, making them vulnerable to extinction. Research can contribute to future conservation actions on behalf of these species by providing accurate information on local distribution and abundance. The distribution of the world’s smallest primate, the endangered Madame Berthe’s mouse lemur (Microcebus berthae), is limited to the Menabe Central region of western Madagascar. This species was discovered in the 1990s, but many fundamental aspects of its ecology remain unknown. The aims of our study were therefore to determine the actual distribution of Microcebus berthae across the forests of this region, to estimate population density, and to examine the species’ response to anthropogenic activities. We established 35 1-km line transects across Menabe Central, on which we surveyed mouse lemurs by distance sampling and live trapping. Microcebus berthae does not occur in all remaining forests of this small region and its population density is highly heterogeneous, both across its geographic range and locally. Within its area of occupancy, the population of Microcebus berthae not only was distributed according to spatial heterogeneities of the habitat, but also responded to anthropogenic disturbances and varied seasonally. Our results indicate that Microcebus berthae is susceptible to habitat degradation and avoids human environments spatially. As none of the forest remnants in which the species still occurs were officially protected until recently, immediate conservation actions should focus on effectively protecting Kirindy and Ambadira forests.     

Bioenergetic Aspects of Halophilism

Examinination of microbial diversity in environments of increasing salt concentrations indicates that certain types of dissimilatory metabolism do not occur at the highest salinities. Examples are methanogenesis for H₂ + CO₂ or from acetate, dissimilatory sulfate reduction with oxidation of acetate, and autotrophic nitrification. Occurrence of the different metabolic types is correlated with the free-energy change associated with the dissimilatory reactions. Life at high salt concentrations is energetically expensive. Most bacteria and also the methanogenic archaea produce high intracellular concentrations of organic osmotic solutes at a high energetic cost. All halophilic microorganisms expend large amounts of energy to maintain steep gradients of NA⁺ and K⁺ concentrations across their cytoplasmic membrane. The energetic cost of salt adaptation probably dictates what types of metabolism can support life at the highest salt concentrations. Use of KCl as an intracellular solute, while requiring far-reaching adaptations of the intracellular machinery, is energetically more favorable than production of organic-compatible solutes. This may explain why the anaerobic halophilic fermentative bacteria (order Haloanaerobiales) use this strategy and also why halophilic homoacetogenic bacteria that produce acetate from H₂ + CO₂ exist whereas methanogens that use the same substrates in a reaction with a similar free-energy yield do not.     

Primate Abundance in an Unhunted Region of the Northern Peruvian Amazon and the Influence of Seismic Oil Exploration

The western Amazon, a relatively remote and unstudied region, is experiencing unprecedented levels of oil and gas exploration. Despite the widespread use of seismic reflection technology for oil and gas exploration, no studies have investigated the response of primate populations to this disturbance in the Amazon. We conducted distance sampling along transects in pristine, unhunted lowland rain forest inside a large oil concession (Block 39) in the northern Peruvian Amazon with ongoing 2D seismic exploration. We aimed to investigate seismic exploration effects on local primate abundance, with a particular focus on the region’s most endangered primates, lowland woolly monkeys (Lagothrix poeppigii) and white-bellied spider monkeys (Ateles belzebuth). We sampled transects before the arrival of exploration crews (control) and during the seismic operation (disturbance) and compared primate counts using mixed-effect models. We confirmed the presence of nine species of primates along sampled transects. Abundance of primate groups (species pooled) was not different between the control and disturbance period, yet abundance of primate individuals was significantly lower in the disturbance period. Although we encountered groups of Ateles belzebuth equally often during the control and disturbance periods, overall counts of individuals of this species were lower during the disturbance period owing to lower subgroup sizes. This suggests this species may have responded, at least temporarily, with localized spatial avoidance, and that it may be particularly sensitive to human disturbance regardless of hunting pressure. Our overall density estimate for Lagothrix poeppigii (30.6/km²) approaches the highest reported for the species. Although the relatively temporary nature of 2D seismic exploration may limit its effect on primate species, our data indicate some species may respond more negatively than others.     

Bioenergetic aspects of halophilism.

Examination of microbial diversity in environments of increasing salt concentrations indicates that certain types of dissimilatory metabolism do not occur at the highest salinities. Examples are methanogenesis for H2 + CO2 or from acetate, dissimilatory sulfate reduction with oxidation of acetate, and autotrophic nitrification. Occurrence of the different metabolic types is correlated with the free-energy change associated with the dissimilatory reactions. Life at high salt concentrations is energetically expensive. Most bacteria and also the methanogenic Archaea produce high intracellular concentrations of organic osmotic solutes at a high energetic cost. All halophilic microorganisms expend large amounts of energy to maintain steep gradients of NA+ and K+ concentrations across their cytoplasmic membrane. The energetic cost of salt adaptation probably dictates what types of metabolism can support life at the highest salt concentrations. Use of KCl as an intracellular solute, while requiring far-reaching adaptations of the intracellular machinery, is energetically more favorable than production of organic-compatible solutes. This may explain why the anaerobic halophilic fermentative bacteria (order Haloanaerobiales) use this strategy and also why halophilic homoacetogenic bacteria that produce acetate from H2 + CO2 exist whereas methanogens that use the same substrates in a reaction with a similar free-energy yield do not.     

Bioenergetic strategy of a xylem-feeder

To understand the efficiency of energy flow through an organism living in a nutrient poor environment, the bioenergetics of a xylem-feeding beetle Aredolpona rubra was investigated. The larvae of different ages were kept at a constant high, constant low and seasonally variable temperature or in agar plates and agar + nitrogen plates. Bioenergetic parameters were measured during the course of 1 year. The results showed (i) a very strong influence of food moisture on the bioenergetic parameters of A. rubra, (ii) the influence of temperature depends on whether it is fluctuating or constant, (iii) opposite mechanisms regulate growth in a shortage of water and at a suboptimal temperature: in the former case, consumption does not change while the metabolic rate decreases, and at a suboptimal temperature the metabolic rate is dictated by temperature and the consumption rate is altered and (iv) a nitrogen-rich diet results in a decreased metabolic rate, suggesting the existence of energetically costly adaptations to low quality wood as a food source. The study results have broad implications for environmental influences on insect life histories.     

Multi-targeted Effect of Nicotinamide Mononucleotide on Brain Bioenergetic Metabolism

Neurochemical Research - Dysfunctions in NAD+ metabolism are associated with neurodegenerative diseases, acute brain injury, diabetes, and aging. Loss of NAD+ levels results in impairment of...     

Primate Cognition

Primate Cognition. Michael Tomasello and Josep Call. New York: Oxford University Press, 1997.518 pp.     

Primate Behavior Studies: Essential to Primate Welfare

A special session of the 2006 Animal Behavior Society annual meeting

In Memory of Sylvia Taylor, DVM     

Primate gloom

A new worldwide survey finds that almost half of all primate species are in danger of becoming extinct. Nigel Williams reports.