Cerebral blood flow rates in recent great apes are greater than in Australopithecus species that had equal or larger brains

Cerebral blood flow rates in recent great apes are greater than in Australopithecus species that had equal or larger brains. Roger S. Seymour, Vanya Bosiocic, Edward P. Snelling, Prince C. Chikezie, Qiaohui Hu, Thomas J. Nelson, Bernhard Zipfel and Case V. Miller. Volume 286, Issue 1915, November 13 2019. https://doi.org/10.1098/rspb.2019.2208

Abstract: Brain metabolic rate (MR) is linked mainly to the cost of synaptic activity, so may be a better correlate of cognitive ability than brain size alone. Among primates, the sizes of arterial foramina in recent and fossil skulls can be used to evaluate brain blood flow rate, which is proportional to brain MR. We use this approach to calculate flow rate in the internal carotid arteries (Q˙ICA), which supply most of the primate cerebrum. Q˙ICA is up to two times higher in recent gorillas, chimpanzees and orangutans compared with 3-million-year-old australopithecine human relatives, which had equal or larger brains. The scaling relationships between Q˙ICA and brain volume (Vbr) show exponents of 1.03 across 44 species of living haplorhine primates and 1.41 across 12 species of fossil hominins. Thus, the evolutionary trajectory for brain perfusion is much steeper among ancestral hominins than would be predicted from living primates. Between 4.4-million-year-old Ardipithecus and Homo sapiens, Vbr increased 4.7-fold, but Q˙ICA increased 9.3-fold, indicating an approximate doubling of metabolic intensity of brain tissue. By contrast, Q˙ICA is proportional to Vbr among haplorhine primates, suggesting a constant volume-specific brain MR.

[Q with a dot is first derivative of Q (rate of change with time, in this case)]

1. Introduction

Brain size is the usual measure in discussions of the evolution of cognitive ability among primates, despite recognized shortcomings [1]. Although absolute brain size appears to correlate better with cognitive ability than encephalization quotient, progression index or neocortex ratio [2,3], an even better correlate might be brain metabolic rate (MR), because it represents the energy cost of neurological function. However, brain MR is difficult to measure directly in living primates and impossible in extinct ones.

One solution to the problem has been to measure oxygen consumption rates and glucose uptake rates on living mammals in relation to brain size and then apply the results to brain sizes of living and extinct primates. Because physiological rates rarely relate linearly to volumes or masses of tissues, any comparison requires allometric analysis. For example, brain MR can be analysed in relation to endocranial volume (≈ brain volume, Vbr) with an allometric equation of the form, MR = aVbrb, where a is the elevation (or scaling factor, indicating the height of the curve) and b is the scaling exponent (indicating the shape of the curve on arithmetic axes). If b = 1.0, then MR is directly proportional to brain size. If b is less than 1, then MR increases with brain size, but the metabolic intensity per unit volume of neural tissue decreases. If b is greater than 1, the metabolic intensity of neural tissue increases. The exponent for brain MR measured as oxygen consumption and glucose use across several mammalian species is approximately 0.86, and the exponent for cortical brain blood flow rate in mammals is between 0.81 and 0.87 [4,5]. The similarity of the exponents indicates that blood flow rate is a good proxy for brain MR in mammals in general. The exponents are less than 1.0, which shows that brain MR and blood flow rate increase with brain size but with decreasing metabolic and perfusion intensities of the neural tissue.

Recent studies show that blood flow rate in the internal carotid artery (Q˙ICA)$({\dot{Q}}_{\mathrm{ICA}})$ can be calculated from the size of the carotid foramen through which it passes to the brain [6]. The artery occupies the foramen lumen almost entirely [7–9], therefore defining the outer radius of the artery (ro), from which inner lumen radius (ri) can be estimated, assuming that arterial wall thickness (ro – ri) is a constant ratio (w) with lumen radius (w = (ro – ri)/ri), according to the law of Laplace. The haemodynamic equation used to calculate Q˙ICA${\dot{Q}}_{\mathrm{ICA}}$ is referred to as the ‘shear stress equation’, and attributed to Poiseuille: Q˙=(τπr3i)/(4η)$\dot{Q}=(\tau \pi r_i^3)/(4\eta )$, where Q˙$\dot{Q}$ is the blood flow rate (cm3 s−1), τ is the wall shear stress (dyn cm−2), ri is the arterial lumen radius (cm) and η is the blood viscosity (dyn s cm−2) [10]. The technique was validated in mice, rats and humans, but was initially criticized [11], defended [12] and subsequently accepted [13]. However, the calculations involved three questionable assumptions: flow in the cephalic arteries conforms to Poiseuille flow theory, arterial wall shear stress can be calculated accurately from body mass (although there is no clear functional relationship between them) and the arterial wall thickness-to-lumen radius ratio (w) was a certain constant derived from only two values in the literature.

We have now made significant advancements to the initial methodology by replacing the shear stress equation, and its assumptions, with a new equation derived empirically from a meta-analysis of Q˙$\dot{Q}$ versus ri in 30 studies of seven cephalic arteries of six mammalian genera, arriving at an allometric, so-called ‘empirical equation’, Q˙$\dot{Q}$ = 155 ri2.49 (R2 = 0.94) [14]. The equation is based on stable cephalic flow rates, which vary little between rest, intense physical activity, mental exercise or sleep [14]. The equation also eliminates reliance on the somewhat tenuous estimation of arterial wall shear stress from body mass. We have also improved the calculation with a more extensive re-evaluation of carotid arterial wall thickness ratio (w = 0.30) from 14 imaging studies on humans (electronic supplementary material, text and table S1 for data and references). The present investigation implements these recent methodological advancements and re-evaluates the scaling of Q˙ICA${\dot{Q}}_{\mathrm{ICA}}$ as a function of Vbr in extant haplorhine primates and in fossil hominins. The point of our study is to clarify these relationships between Homo sapiens, Australopithecus and modern great apes (Pongo, Pan, Gorilla) to resolve an apparent allometric conundrum within our previous studies: one analysis based on 34 species of extant Haplorhini, including H. sapiens, resulted in the equation Q˙ICA =8.82×10−3${\dot{Q}}_{\mathrm{ICA}}\hspace{0.17em}=8.82\times {10}^{-3}$Vbr0.95 [6], while another analysis of 11 species of fossil hominin, also including H. sapiens, produced the equation Q˙ICA=1.70×10−4${\dot{Q}}_{\mathrm{ICA}}=1.70\times {10}^{-4}$Vbr1.45 [15]. Humans are on both analyses with the largest brains, but the exponents of these equations are markedly different, and the lines converge. The present study confirms that hominin ancestors had lower Q˙ICA${\dot{Q}}_{\mathrm{ICA}}$ than predicted from Vbr with the haplorhine equation. Q˙ICA${\dot{Q}}_{\mathrm{ICA}}$ in modern great apes is about twice that in Australopithecus species, despite similar or smaller Vbr.

Earth's earliest and deepest purported fossils may be iron-mineralized chemical gardens; then, should not be assumed to represent fossil microbes without independent corroborating evidence

Earth's earliest and deepest purported fossils may be iron-mineralized chemical gardens. Sean McMahon. Proceedings of the Royal Society B, Volume 286, Issue 1916, November 27 2019. https://doi.org/10.1098/rspb.2019.2410

Abstract: Recognizing fossil microorganisms is essential to the study of life's origin and evolution and to the ongoing search for life on Mars. Purported fossil microbes in ancient rocks include common assemblages of iron-mineral filaments and tubes. Recently, such assemblages have been interpreted to represent Earth's oldest body fossils, Earth's oldest fossil fungi, and Earth's best analogues for fossils that might form in the basaltic Martian subsurface. Many of these putative fossils exhibit hollow circular cross-sections, lifelike (non-crystallographic, constant-thickness, and bifurcate) branching, anastomosis, nestedness within ‘sheaths’, and other features interpreted as strong evidence for a biological origin, since no abiotic process consistent with the composition of the filaments has been shown to produce these specific lifelike features either in nature or in the laboratory. Here, I show experimentally that abiotic chemical gardening can mimic such purported fossils in both morphology and composition. In particular, chemical gardens meet morphological criteria previously proposed to establish biogenicity, while also producing the precursors to the iron minerals most commonly constitutive of filaments in the rock record. Chemical gardening is likely to occur in nature. Such microstructures should therefore not be assumed to represent fossil microbes without independent corroborating evidence.

3. Discussion

(a) Comparison with previously reported biomorphs

Here, I have shown that the reaction of ferrous sulfate grains with sodium carbonate and sodium silicate solutions in shallow vessels (Petri dishes, limiting vertical extension and introducing an effect of surface tension) allows for the rapid production of large populations of straight and curved filaments with consistently microbe-like sizes and morphologies, including circular cross-sections, non-crystallographic bifurcation during growth, anastomosis, and nestedness. Compositionally, these biomorphs are typical of iron-based chemical gardens previously described in the experimental literature. Most previous experimental studies following the ‘classic’ procedure have used salt granules or pellets several millimetres in diameter immersed beneath several centimetres of solution within test tubes or similar reaction vessels (e.g. [32–35]). This method produces vertically oriented, chimney-like structures several centimetres in length controlled by buoyancy-driven extension, commonly with several sub-vertical branches, which do not closely resemble candidate fossils in their overall morphology. Other studies have used vertically confined spaces to produce smaller, quasi-2D chemical gardens that form meandering filaments with infrequent branching [42,43]. Interestingly, one of these studies [43] describes self-avoidance during filament growth that would seem to preclude anastomosis. In the present study, anastomosis was present but rare, and filaments sometimes met and grew along with each other as if mutually adhesive but unable to converge into a single filament.

The present results do not exhaust the morphospace accessible to chemical gardens, which can also produce pseudoseptate filaments and spherical bulbous terminations resembling fungal sporangia (e.g. figures 38, 39, 48, 55, and 56 in [44]). Serially twisted/helical filaments or ‘stalks’ of iron oxide, which are widely regarded as biosignatures for iron-oxidizing bacteria (e.g. [28]) were not produced in the present study, but classic work suggests that serially twisted forms can also occur (e.g. figure 55a in [44]). Silica-carbonate biomorphs also show helical forms, and further extend the morphospace of abiotic mineral growth structures to encompass fractally branching dendrites, framboid-like masses, rope-like twisted threads and ribbons, and complex shapes resembling urns, corals, and snails, but not closely resembling the iron-mineral filaments addressed by this study [45,46].

(b) Comparison with iron-mineral filaments in the rock record

Iron-mineral filament assemblages previously interpreted as fossilized microbial populations are composed largely of hematite (e.g. [1,2,7,8,11,15]), iron oxyhydroxides such as goethite and ferrihydrite (e.g. [2,5,7,8,10–12,28]), and iron-rich aluminosilicate clay minerals [6–8,10,25]. In line with previous studies of tubular chemical gardens using iron salts [30,32,33], the Raman, EDX, and XRD analyses in the present study suggest that biomorphs produced by reacting ferrous sulfate with either sodium carbonate or sodium silicate solutions were composed largely of iron oxyhydroxides. These minerals very readily transform to hematite during diagenesis or metamorphism, and may also serve as precursors to Fe-rich phyllosilicates in hydrothermal, silica-rich settings [47,48]. Bacterial iron oxidation can likewise produce iron (oxyhydr)oxides (e.g. [49]), but the present results show that the composition of iron-mineral filaments in the rock record is equally consistent with origination through abiotic processes. A recent study also interpreted hollow silica tubes from hydrothermal deposits of the Arctic Mid-Ocean Ridge as possible chemical gardens [28]; such tubes may be obtainable from experiments like those reported here if terminated before iron oxyhydroxides encrust the initial siliceous membranes; cf. the outer layer in figure 1d [32,33].

When produced from seed grains sieved to less than 63 µm in diameter, 188 out of 200 individual chemical garden filaments measured in this study showed external diameters between 2 and 10 µm (median 3.9 µm); no filaments were narrower than 1 µm, and only four were wider than 12 µm (electronic supplementary material, figure S1). This size distribution and range are similar to numerous assemblages of iron-mineral filaments in the rock record (e.g. [1,6,7,50–52]). The chemical gardens in this study (figure 1) also reproduce almost the full range of morphological characteristics (straight and curved trajectories with changes of direction; filled and unfilled (hollow) interiors; circular cross-sections; multiple attachment to knobs; discrete swellings; non-crystallographic, constant-thickness branching; anastomosis; nestedness) previously thought to show that naturally occurring iron-mineral filaments are likely to be microfossils (e.g. [1,2,4,6–15]). It is important to concede that I did not produce true septate filaments with internal, walled compartments, a feature which has been observed in some natural iron-mineral filament assemblages where carbonaceous residues provide additional evidence for biogenicity (e.g. [9,19,20]). Additionally, although filament thickness was usually conserved during growth even during branching and anastomosis (e.g. figure 1e,f,g), this was not always the case; bifurcation could reduce filament thickness while re-convergence could increase it, leading to some dubiously lifelike morphologies, especially in larger filaments. In addition, some filaments tapered gradually in the direction of growth (e.g. figure 1j).

These results are strikingly similar to the assemblage of hematite tubes and non-septate filaments in hydrothermal chert beds of the 4.0 ± 0.3 giga-annum (Ga) Nuvvuagittuq Greenstone Belt, northeast Canada, recently interpreted as Earth's oldest body fossils [1]. The filaments are reportedly 2–14 µm in diameter and up to 500 µm in length, and have been interpreted as the partly permineralized, partly encrusted remains of iron-oxidizing bacteria [1]. Some filaments are attached to knobs 80–120 µm in diameter, and some are nested within tubes (16–30 µm in diameter and 80–400 µm in length), which also occur without filaments; these features were considered incompatible with an abiotic origin, but are replicated abiotically in the present study (figure 1e,i). Buoyancy- or flow-driven growth of chemical gardens from fairly uniform parent crystals or grains would also explain the straight, unbranched, parallel nature of some of the Nuvvuagittuq tubes and their consistent sizes. Hollow tubes could also have originated via dissolution, diffusion, and re-precipitation of filaments during the polymerization of the surrounding silica, with or without leaving residual filaments inside; filaments in some moss agates are surrounded by (commonly multiple) concentric sheath-like tubes likely to have formed similarly [53,54]. Other evidence adduced to support the biogenicity of the Nuvvuagittuq filaments (e.g. the presence near the filaments of graphite, carbonate rosettes with isotopically light carbon, and phosphate) does not settle the biogenicity of the filaments themselves, which are morphologically simple and strictly non-carbonaceous. It is not implausible that alkaline fluids generated by serpentinization of the mafic (sub)seafloor promoted the growth of chemical gardens in this setting.

The results are also reminiscent of numerous candidate microfossils proposed to have formed in subsurface environments, i.e. the deep biosphere (e.g. [5–10,50,51]; see review in [18]). Among these, one assemblage of special scientific importance is the suite of iron-rich chloritic filaments preserved within calcite- and chlorite-filled amygdales (mineralized vesicles) in basalts from the lower part of the 2.4 Ga Ongeluk Formation of South Africa [6]. These filaments were recently interpreted as the oldest fossil eukaryotes, but are similar to the chemical gardens described in the present study in several respects. They are solid, apparently non-septate, about 2–12 µm in diameter, and up to hundreds of µm in length. They are composed of iron-rich chlorite, a common vein- and amygdale-filling phyllosilicate in hydrothermally altered basaltic rocks, where it also forms the filamentous dubiofossil ‘moss’ found in moss agates [55]. The origin of the Ongeluk chlorite is not precisely known; it could derive from the alteration of smectite that replaced organic matter as proposed by Bengtson et al. [6], but smectite can also form via the interaction of hydrothermal silica and iron oxyhydroxides, i.e. the constituents of chemical garden filaments [48]. Independent evidence for an influx of silica-rich hydrothermal fluids exists in the lower part of the Ongeluk Formation in the form of abundant hydrothermal jasper and chert deposits [56].

While the composition of the Ongeluk filaments is seemingly compatible with both biotic and abiotic interpretations, the argument that they are biotic rests largely on their morphological and organizational resemblance to putative fossil fungi from much younger rocks (including some that preserve organic matter). The Ongeluk filaments show curvilinear trajectories, branching, anastomosis, circular cross-sections, and bulbous protrusions. The results of the present study show that all these features are equally consistent with chemical garden growth. Neither the radiating growth of filaments inwards from cavity walls (also seen in moss agates) nor the occurrence of multifurcate, entangled ‘broom’ structures [6] was replicated in my Petri dish experiments, but these features do not seem fundamentally incompatible with chemical garden growth provided with the appropriate distribution of seed material and the correct flow regime and rate. Chemical garden filaments are flexible in the early, gelatinous phase of growth and can become entangled during growth with or without anastomosing. The irregular chlorite lining Ongeluk amygdales, described by Bengtson et al. [6] as a ‘basal film consisting of a jumbled mass', could represent an amalgamation of the membranes formed around seed material in chemical gardens, which become mineralized along with the filaments (figure 1e,g). More naturalistic experimental systems must be used to test these proposals before the hypothesis that the Ongeluk filaments represent chemical gardens can be evaluated fully.

(c) Plausibility of chemical garden growth in nature

Chemical gardens are already thought to occur in geological settings where silica and/or carbonate-laden alkaline fluids react with metalliferous mineral particles or solutions, most notably forming complex structures at marine hydrothermal vents (e.g. [28]; see also [32] for a discussion of chemical gardens in nature). Deep, isolated groundwater tends to become somewhat alkaline (as well as carbonate- and silica-rich) as a consequence of water–rock reactions that consume H+, and in some settings the hydrolysis of olivine and pyroxene in basalts and ultramafic rocks (serpentinization) leads to groundwater pH values as high as 10–12.6 [48,57–61]. Lakes fed by hydrothermal systems in the East African Rift Valley are sufficiently alkaline and silica-rich to be theoretically compatible with biomorph production at the Earth's surface [46], and it has recently been demonstrated experimentally that naturally occurring silica-rich alkaline spring waters are capable of inducing the growth of classical chemical gardens from iron salts, as well as producing silica-carbonate biomorphs [35]. Moreover, the results presented here show that very high pH is not required to form microbe-like filaments, which grew in sodium carbonate solutions acidified to mildly alkaline and even neutral pH (figure 3). Thus, it is reasonable to suppose that groundwater in many of the settings where iron-mineral filament assemblages have been found—silicifying/calcifying marine hydrothermal systems, volcanic rocks near mid-ocean ridges and deeply buried on land, and limestones—could have become sufficiently alkaline to precipitate iron-mineral chemical garden filaments. Further experimental work is, however, needed to test this supposition. Since naturally occurring iron-mineral filaments are widely associated with the common ferrous sulfide mineral, pyrite (e.g. [4,7,62]), I further speculate that the ferrous sulfate minerals or solutions derived from the oxidation of iron sulfide minerals (not necessarily abiotically) may have stimulated the formation of filamentous chemical gardens in some natural settings (a pyrite precursor for some moss agates was also suggested by Hopkinson et al. [27]).

(d) Discriminating between iron-mineralized chemical gardens and fossil microbes

Some natural iron-mineral filament assemblages contain complex organic matter and phosphate, together with iron-mineral growth-textures strongly suggestive of encrustation onto pre-existing organic material, implying that they are more likely to be fossils than not (e.g. [63,64]). Filaments associated with carbonaceous material of indeterminate origin are not necessarily biogenic [31], and most iron-mineral filament assemblages lack such material altogether. Nevertheless, iron-encrusted microbial filaments and abiotic chemical garden filaments and tubes are unlikely to be perfectly indistinguishable in composition, morphology, texture, or organization at all scales, and the possibility remains that diagnostic differences may be discovered [28]. Statistical analyses of morphometric parameters over large populations of biotic and abiotic filaments may be fruitful; preliminary steps have been taken in this direction (e.g. [8,28,45,52]). The controlled experimental iron-mineral encrustation of large numbers of bacterial and fungal filaments will be necessary to provide suitable datasets. As a corollary, experiments to grow chemical gardens in the presence of filamentous microbes may be worthwhile in case this leads to new morphologies. Submicroscopic internal and external textures of biotic and abiotic filaments, not explored in detail by the present work, should be compared. Both smooth-walled and more coarsely crystalline tubes and filaments are found in natural iron-mineral filament assemblages, even together within the same assemblage (e.g. [1]). In the present study, abiotic filaments grown in sodium silicate solution showed smoother exteriors than those produced in sodium carbonate. Smoothness has recently been shown to respond to growth rate, with slow-forming chemical garden filaments tending to show more coarsely textured walls [65]; it has also been shown that chemical gardens grown from ferrous chloride differ microtexturally (and mineralogically) from their ferric equivalents [34]. It was recently pointed out [28] that concurrent precipitation of silica and iron minerals might produce a diagnostically abiotic internal structure in some natural filament assemblages, i.e. a diffuse filament core zone composed of iron-mineral spherules supported by a silica matrix; this was not observed in the present study, but might perhaps occur if more highly polymerized silica media were used.