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.

Pathogen defence is a potential driver of social evolution in beetles: Daughters prolonged their cooperative phase within their mothers' nest, increasing hygienic behaviors (allogrooming & cannibalism)

Pathogen defence is a potential driver of social evolution in ambrosia beetles. Jon A. Nuotclà, Peter H. W. Biedermann and Michael Taborsky. Proceedings of the Royal Society B, Volume 286, Issue 1917, December 18 2019. https://royalsocietypublishing.org/doi/10.1098/rspb.2019.2332

Abstract: Social immunity—the collective behavioural defences against pathogens—is considered a crucial evolutionary force for the maintenance of insect societies. It has been described and investigated primarily in eusocial insects, but its role in the evolutionary trajectory from parental care to eusociality is little understood. Here, we report on the existence, plasticity, effectiveness and consequences of social pathogen defence in experimental nests of cooperatively breeding ambrosia beetles. After an Aspergillus spore buffer solution or a control buffer solution had been injected in laboratory nests, totipotent adult female workers increased their activity and hygienic behaviours like allogrooming and cannibalism. Such social immune responses had not been described for a non-eusocial, cooperatively breeding insect before. Removal of beetles from Aspergillus-treated nests in a paired experimental design revealed that the hygienic behaviours of beetles significantly reduced pathogen prevalence in the nest. Furthermore, in response to pathogen injections, female helpers delayed dispersal and thus prolonged their cooperative phase within their mother's nest. Our findings of appropriate social responses to an experimental immune challenge in a cooperatively breeding beetle corroborate the view that social immunity is not an exclusive attribute of eusocial insects, but rather a concomitant and presumably important feature in the evolutionary transitions towards complex social organization.

1. Introduction

Pathogens pose a major risk to highly social animals. Insect societies, for instance, provide ideal conditions for their dissemination [1,2], because a large number of closely related individuals with potentially very similar immune defences live together in intimate contact and under homogeneous, environmentally buffered conditions. Low genetic variance has been shown to reduce the chances of successfully resisting severe fungus infections in honeybees, and in ants it reduces the effectiveness of anti-pathogen behaviours [3,4]. To counter pathogen risk, social insects evolved various physiological and behavioural strategies to inhibit the spread of diseases [5].

The innate immune system, pathogen avoidance and self-cleaning behaviours are probably the most common anti-pathogen strategies in insects. In addition to such traits that might be termed ‘non-social’, many social insects were found to express social immunity, which refers to cooperative sanitation involving the joint mechanical and chemical removal of bacterial and fungal pathogens. Originally, social immunity was regarded as a nest-wide parasite and pathogen defence mechanism that evolved in eusocial insects to counter the beforementioned inherent risks of infection caused by the social lifestyle and genetic homogeneity [5]. Importantly, this concept has highlighted the parallels between the innate non-social immune system of a single multicellular organism and a nest-wide ‘social immune system’ of a complex insect society. This idea relates to the concept of superorganismality, where a whole nest of social insects is regarded as a single reproducing entity (the ‘super organism’ [6,7]). Groups of nest members take on specialized roles, which corresponds to the differentiated cell tissues of a multicellular organism [8,9]. In the best-studied societies of ants and bees, for example, this is proposed to have led to the evolution of sophisticated group-level social immune defences by workers, including application of antimicrobial substances onto contaminated areas, removal of corpses and diseased brood, social fever and allogrooming [10–12]. Such sanitation behaviour is not restricted to eusocial insects, however, as its precursors are already present in subsocial insects with parental care (e.g. [13–15]), although empirical data from such systems are scarce. This sparked a debate about whether the concept of social immunity should be extended to include cooperative sanitation tasks performed in non-eusocial group living species, to better understand the evolutionary origins of social immunity [11,16].

This recent debate highlights that the evolution of social immunity is hitherto unclear. Either social immunity evolved as a result of increased pathogen transmission in eusocial organisms (termed the eusocial framework [5,11,16]) or sociality and social immunity co-evolved in a close feedback interaction (termed the group living framework [15–17]). In some taxa, the suppression of pathogens is a very important social task, not only exhibited by parents towards offspring, but sometimes even between all individuals in a nest or aggregation. Hence, it is conceivable that under certain circumstances, pathogens themselves may be important drivers of sociality. This might be true especially in taxa that live in permanent close contact to a decaying food source and are thus frequently in contact with various microbes (e.g. involving parental care in burying beetles, larval aggregations in Drosophila or worker specialization in attine ants [17]). Our study explored this possibility further by introducing fungus-farming bark beetles as a system for the experimental study of social immunity.

These so-called ambrosia beetles offer a unique opportunity for studying the evolution of social traits because closely related species express various social structures ranging from uniparental care to eusociality [18]. Cooperative breeders are of particular interest for experimentally studying social evolution, as here adult females delay dispersal and act as helpers or temporary workers. The length of dispersal delay is affected by the presence and quantity of dependent offspring in the colony and the level of nutrition [19,20], but it might also be affected by the presence and load of pathogens.

All ambrosia beetles live in close mutualistic relationships with different fungi and bacteria, which they farm as their sole source of nutrition within tunnel systems in the heartwood of trees. The main mutualists are so-called ambrosia fungi, primarily from the ascomycete orders Microascales and Ophiostomatales [21–23]. These fungi are taken up from the natal nest by dispersing adult females in special spore carrying organs called mycetangia and subsequently spread on the walls of newly excavated tunnel systems. Finally, they are cultivated and possibly protected from other (fungal) pathogens or competitors [18,23,24]. In addition to these fungal mutualists, several other fungi have been isolated from beetle nests, many of which are pathogens for the beetles or at least competitors of the beetles' fungal mutualists [21,23]. The genera Aspergillus and Beauveria, for example, can directly infect and kill adults and brood of ambrosia beetles [23,25–28]. Other fungi compete with the ambrosia fungi and thus deplete the food source of the beetles (e.g. Penicillium sp., Chaetomium sp., Nectria sp. [29]). Such pathogens and competitors are probably the primary threat for the beetles because within the wood, they are well protected from most other natural enemies.

Morphological castes such as those in eusocial insects do not exist in ambrosia beetles. Instead, many species show division of labour among totipotent adult and larval offspring, with adults overtaking nest protection and sanitation, and larvae engaging in nest enlargement and packing of frass (i.e. sawdust, faeces and possibly pathogens) [19]. Larvae and adults join forces to pack and expel pellets of waste through the nest entrance. One of the most common behaviours in both adults and larvae is allogrooming of each other and the brood, probably against pathogens. Diseased individuals are either cannibalized or removed from the nest [19]. Currently, it is unknown, however, if ambrosia beetle larvae and/or adults can detect pathogens and actively suppress their load within nests. Some bark beetles have been shown to exude secretions from their mouth to kill pathogenic fungi [30]. Others, like the species Dendroctonus frontalis, are associated with bacteria that produce antibiotics which selectively kill antagonistic microorganisms threatening their fungal associates [31]. Indications for such a bacterial defence mechanism that specifically targets fungal pathogens and not the fungal cultivars have been recently also found in our model species Xyleborinus saxesenii [32].

Recent advancements in laboratory rearing, observation and in situ manipulation techniques [24,33,34] allow studies of social pathogen defence in ambrosia beetles. Previous studies revealed vigorous cleaning behaviours by adult offspring and even larvae. Since all ambrosia beetles live in close contact to a rich microbial environment, similar to some of the best-described models for social immunity in eusocial insects, we expect to find convergent behavioural adaptations to increased pathogen exposure. In addition, the naturally very high inbreeding rate found in cooperatively breeding ambrosia beetles is assumed to create a condition similar to eusocial insects, where the genetic homogeneity of nestmates renders group members highly vulnerable to microbial attack.

To test this idea, we used the cooperatively breeding and naturally highly inbred species X. saxesenii Ratzeburg to determine the effect of Aspergillus fungal pathogens on beetle social behaviours and potential social immunity. This pathogen was chosen because it has been repeatedly isolated from diseased individuals from X. saxesenii nests (see electronic supplementary material, figure S1) and it is well known for its pathogenicity for many insects (including other bark beetles [26,27]), which is a result of produced aflatoxins [35,36]. Aspergillus spores were experimentally injected in laboratory nests, and effects were determined on (i) the social behaviours displayed by larvae and adults and (ii) the timing of dispersal of adult offspring from the natal nest. In addition, (iii) we assessed the effectiveness of the beetles' hygienic behaviours on pathogen spore loads, by comparing pathogen spore loads of nest parts with beetles present against parts where beetles had been experimentally removed after injection of the pathogen. We predict that the group members increase nest sanitation in response to the introduced pathogen and that this behaviour reduces pathogen spore loads. Furthermore, daughters will either delay their dispersal to help with nest hygiene and thus increase their indirect fitness benefits or disperse earlier to protect their individual health and direct fitness gains.

Deconstructing sociality: the types of social connections that predict longevity in a group-living primate

Deconstructing sociality: the types of social connections that predict longevity in a group-living primate. Samuel Ellis, Noah Snyder-Mackler, Angelina Ruiz-Lambides, Michael L. Platt and Lauren J. N. Brent. Proceedings of the Royal Society B, Volume 286, Issue 1917, December 18 2019. https://royalsocietypublishing.org/doi/10.1098/rspb.2019.1991

Abstract: Many species use social interactions to cope with challenges in their environment and a growing number of studies show that individuals which are well-connected to their group have higher fitness than socially isolated individuals. However, there are many ways to be ‘well-connected’ and it is unclear which aspects of sociality drive fitness benefits. Being well-connected can be conceptualized in four main ways: individuals can be socially integrated by engaging in a high rate of social behaviour or having many partners; they can have strong and stable connections to favoured partners; they can indirectly connect to the broader group structure; or directly engage in a high rate of beneficial behaviours, such as grooming. In this study, we use survival models and long-term data in adult female rhesus macaques (Macaca mulatta) to compare the fitness outcomes of multiple measures of social connectedness. Females that maintained strong connections to favoured partners had the highest relative survival probability, as did females well-integrated owing to forming many weak connections. We found no survival benefits to being structurally well-connected or engaging in high rates of grooming. Being well-connected to favoured partners could provide fitness benefits by, for example, increasing the efficacy of coordinated or mutualistic behaviours.

4. Discussion

By quantifying the relationship between survival and four of the most common operational definitions of social connectedness in a single system, this study highlights the fact that being ‘well-connected’ is multi-faceted in nature and provides evidence that some aspects of sociality represent more straightforward routes to biological success than others. In particular, we found support for a relationship between survival and dyadic connectedness: adult female rhesus macaques that frequently interacted with their top partners and that had partners that were stable over time were more likely to survive than females which interacted less often with their preferred and stable partners. However, we found no relationship between a female's number of strong connections and her probability of survival. For dyadic connections, at least, it appeared as though quality was more important than quantity. We also found some support for a relationship between social integration and survival: females that had a large number of weak connections experienced a lower mortality hazard. Other predictions of the social integration hypothesis were not supported, and there was little evidence that being structurally or directly well-connected resulted in survival benefits.

Our results add to previous studies linking the quality of dyadic relationships with positive fitness outcomes in social animals (table 1). In this study, rhesus macaque females with the strongest connections to their top partner had an 11% higher probability of survival than females that were less well-connected to their top partner. Repeatedly interacting with the same small number of individuals may facilitate the emergence and maintenance of cooperative relationships, whereby partners exchange behavioural services, such as grooming and coalitionary support, and where the consistency of partner identity may improve coordination of those behaviours and deter cheating [60,61].

Consistent and frequent partners may also result in benefits related to mutual social tolerance. In despotic, hierarchical, societies, like those of many female Old World primates, tolerated access to necessary resources, including food and space, may be beneficial to individuals [62–64]. Repeated and stable partnerships may initially arise because of shared needs or preferences amongst pairs of individuals. For example, individuals with similar metabolisms, thermoregulatory needs, or preferences for certain foods, may repeatedly find themselves attempting to access the same resource [65,66]. If alliances between pairs of individuals result in tolerance of that pair when accessing a resource, combined with mutualistic joint defence of that resource against competing groupmates, repeated and stable relationships may emerge. This scenario relies on relative stability in resource availability and in individual differences in needs and preferences. Individuals living outside of those conditions may have little need for stable partners, and may therefore exhibit a divergent relationship between dyadic connectedness and fitness [22,23,30]. In these species, a more flexible and generalized strategy of connectedness—via, for example, social integration—may be a better strategy for coping with the challenges of group-living.

In addition to dyadic connectedness, we found that some aspects of social integration predicted survival in this study; the number of weak connections a female maintained was linked to her mortality hazard. Wide social tolerance derived from these connections may allow a female to feed without disturbance or avoid harassment in a greater number of settings than females with fewer weak connections. Similar to the results presented here, blue monkeys (Cercopithecus mitis) survival has been shown to be positively associated with both strong-consistent connections and weak-inconsistent connections [51]. In the current population of rhesus macaques, measures of social integration have been positively linked to reproductive output [12] and proxies of social integration (family size) have been linked to survival [6]. Interestingly, correlations (electronic supplementary material, figure S1) and principal component analysis (electronic supplementary material, figure S6) suggest that dyadic connectedness measures and social integration measures are negatively associated in this population. That is, females with strong dyadic connectedness tend to have weak social integration. Taken together, these results may suggest that both dyadic connectedness and social integration can provide fitness benefits (albeit perhaps of different types) within the same system.

There was quantitative and qualitative variation in the relationship between survival and a female's number of strong connections, and between survival and number of weak connections depending on the threshold used to define connections as strong or weak. Choice of the threshold can, therefore, have important implications for the conclusions reached by a study, and we suggest that thresholds either be based on features of the data or behaviour of study species. More generally, connectedness is an individual effect. Defining connections as strong or weak at the population level and then calculating connectedness at the individual level may not best represent the salient features of the social environment experienced by individuals. This is highlighted by our contrasting results for number of strong connections and strength of connection to top associates (which is a measure defined at the individual level).

We found no evidence of a relationship between an individual's position in the broader social network and their probability of surviving. Individuals that are well-connected to their broader social worlds have been suggested to benefit from being among the first to receive useful information when it enters the system. For example, in resident-ecotype killer whales, indirect network position predicts male survival, potentially because well-positioned males are more likely to receive information about the presence and location of resources [13]. The rhesus macaques in our study were provisioned at regular intervals and predictable locations and have no predators. The opportunities for individuals to gain survival benefits from social information in this population may, therefore, be limited. Although information about the social environment such as mating opportunities, changes in group membership or dominance rank, are probably important for the success of these animals, the benefits of this information might be more tightly born out in terms of reproductive success [12] and less so in terms of survival.

Measures of direct connectedness were also not important predictors of survival in female rhesus macaques: neither a greater amount of time spent in proximity to others, engaged in grooming, nor the relative amount of grooming received were associated with increased probability of survival. In some primate species, grooming rates have been linked to lower parasite loads (e.g. [35]). Our findings suggest that the benefits of sociality are not directly derived from the behaviours involved in sociality, at least in this population. This interpretation aligns with suggestions that relationships are a commodity or resource that are promoted and maintained in some social animals.

Other social factors not considered in detail here are also likely to influence mortality. Dominance rank has been shown to be an important predictor of fitness and health (e.g. [10]) and a source of variation in social behaviour [67]) in primates, including in rhesus macaques [6,42,68]. Dominance rank did not significantly predict survival when evaluated as a term on its own and it was therefore not included as a main effect in subsequent models. Dominance rank was also not included as an interaction term with social connectedness because of concerns of overfitting. The analyses—in essence—represent the fitness consequences of sociality in females of ‘average’ rank. Including the interaction between connectedness and rank in future analyses may reveal important subtleties in the relationship between sociality and fitness. It is conceivable, for example, that the importance of social connectedness differs for females of high and low rank, though it should be noted that including rank has increased the observed benefits of sociality in this study system [6]. Further analyses based on longer observations and increased sample sizes would be needed to reveal how rank, and other behavioural and ecological constraints, influence the relationship between connectedness and longevity.

Overall, the results presented here demonstrate the value of understanding what exactly is meant by being ‘socially well-connected’. Although ‘sociality’ and ‘connectedness’ are useful catch-all terms, the methods used to measure them can influence results revealed and the conclusions reached. We have highlighted how different aspects of sociality can result in different biological conclusions. Future work in other species is needed to understand the generality of the conclusions reached here. Testing whether different conceptualizations of being well-connected are related to proxies of fitness other than survival, such as reproductive success, are also required, as are studies investigating how different aspects of connectedness interact in other systems.

One unique feature of digital emotion contagion is that it is mediated by digital media platforms that are motivated to upregulate users’ emotions

Goldenberg, Amit, and James Gross. 2019. “Digital Emotion Contagion.” OSF Preprints. October 2. doi:10.31219/osf.io/53bdu

Abstract: People spend considerable time on digital media, and during this time they are often exposed to others’ emotion expressions. This exposure can lead their own emotion expressions to become more like others’ emotion expressions, a process we refer to as digital emotion contagion. This paper reviews the growing literature on digital emotion contagion. After defining emotion contagion, we suggest that one unique feature of digital emotion contagion is that it is mediated by digital media platforms that are motivated to upregulate users’ emotions. We then turn to measurement, and consider the challenges of demonstrating that digital emotion contagion has occurred, and how these challenges have been addressed. Finally, we call for a greater focus on understanding when emotion contagion effects will be strong versus weak or non-existent.

Killfish evolution of brain cell proliferation: More plasticity according to a higher degree of predation

Predation drives the evolution of brain cell proliferation and brain allometry in male Trinidadian killifish, Rivulus hartii. Kent D. Dunlap, Joshua H. Corbo, Margarita M. Vergara, Shannon M. Beston and Matthew R. Walsh. Proceedings of the Royal Society B, Volume 286, Issue 1917, December 18 2019. https://doi.org/10.1098/rspb.2019.1485

Abstract: The external environment influences brain cell proliferation, and this might contribute to brain plasticity underlying adaptive behavioural changes. Additionally, internal genetic factors influence the brain cell proliferation rate. However, to date, researchers have not examined the importance of environmental versus genetic factors in causing natural variation in brain cell proliferation. Here, we examine brain cell proliferation and brain growth trajectories in free-living populations of Trinidadian killifish, Rivulus hartii, exposed to contrasting predation environments. Compared to populations without predators, populations in high predation (HP) environments exhibited higher rates of brain cell proliferation and a steeper brain growth trajectory (relative to body size). To test whether these differences in the wild persist in a common garden environment, we reared first-generation fish originating from both predation environments in uniform laboratory conditions. Just as in the wild, brain cell proliferation and brain growth in the common garden were greater in HP populations than in no predation populations. The differences in cell proliferation observed across the brain in both the field and common garden studies indicate that the differences are probably genetically based and are mediated by evolutionary shifts in overall brain growth and life-history traits.

1. Introduction
Researchers have devoted much attention to assessing whether changes in adult neurogenesis in response to the environment might be a mechanism of adaptive brain plasticity [1,2]. While the precise functional significance of adult neurogenesis is still debated, there is substantial evidence from many model systems that environmental stimuli alter neurogenic rates in specific brain regions, and that such neurogenic changes have behavioural consequences [3]. For example, complex odour environments increase neurogenesis in the olfactory bulb of rodents [4], and these new neurons enhance odour discrimination abilities [5]. Similarly, seasonal changes in day length promote neurogenesis in the song nuclei in the brains of several bird species, and these neurons are linked to seasonal song production [6].

Most of our understanding of environmental influences on adult neurogenesis comes from laboratory studies in which researchers manipulate environmental stimuli and document effects over the timescale of days to months. That is, they demonstrate an external factor driving phenotypic plasticity in the neurogenic rate. However, the neurogenic rate can also be influenced by intrinsic genetic factors [7–9], and thus, over evolutionary timescales, the environment can modify the neurogenic rate via natural selection acting within populations. Selection could act directly on the neurogenic rate if enhanced (or reduced) brain plasticity confers an advantage in responding to environmental change. Additionally, in species with indeterminate growth, such as most fishes, the brain grows in tandem with the body throughout adulthood [10,11], and selection on body growth trajectories could indirectly affect brain growth and the underlying cellular processes of brain growth [12]. Thus, population variation in the neurogenic rate could arise from phenotypic responses to different environments, or from evolved genetic divergence owing to direct selection on brain growth rate or as an indirect, correlated response to selection on body growth (figure 1). We evaluated these alternative explanations by examining one stage of adult neurogenesis, brain cell proliferation, in killifish (Rivulus hartii) populations from different predator environments. By measuring brain cell proliferation rates in populations exposed to differential predation pressure in the field as well as those same populations reared in a common laboratory environment, we assessed whether population variation in brain cell proliferation is attributable to natural environmental differences versus intrinsic population differences. Finally, we evaluated the predator effects on brain cell proliferation within the context of lifetime growth trajectories of the brain and body in populations [13–16] to assess how population variation in brain cell proliferation fits into the overall evolved difference in life history.

[Figure 1. Three alternative causal chains linking the environment with variation in brain cell proliferation.]

In Trinidad, R. hartii are found in sites where they are the only species present (Rivulus only (RO) sites) and lack predators as well as in sites where they are exposed to predatory fish such as Hoplias malabaricus and Crenicichla frenata (high predation (HP) sites). RO sites are typically located upstream from HP sites above barrier waterfalls that truncate the distribution of large piscivores [13,14,16,17]. These sites are located near each other and thus do not differ in physical habitat and environmental variables (i.e. water temperature and dissolved oxygen) [14]. In HP sites, Rivulus suffer increased mortality, are found at lower densities, and, in turn, they exhibit faster rates of individual growth (HP sites also have a more open canopy) [13,18]. Rivulus can also be bred and reared in the laboratory, allowing us to identify intrinsic (probably genetic) differences between populations that are independent of the environment, and many previous studies have indeed demonstrated that increased predation pressure is associated with evolutionary changes in life-history traits [13,15,19].

Recent work on Rivulus showed that divergent patterns of predation lead to evolutionary shifts in brain size [20]. Increased predation rates in HP sites are associated with the evolution of smaller brains in male (but not in female) Rivulus. Given this negative association between predator environment and brain size in male Rivulus and the negative effect of predators on brain cell proliferation in another freshwater teleost [21,22], we predicted that Rivulus from HP populations would have lower rates of brain cell proliferation than those from RO populations. In fact, we found the opposite: brain cell proliferation was higher in HP populations than in RO populations. These differences were maintained in first-generation laboratory-reared fish, indicating that they probably arise from evolved genetic divergence rather than through phenotypic plasticity. Population differences in cell proliferation were found across all sampled brain regions and correlated with population differences in overall brain allometry, suggesting that they evolved as part of broader evolutionary changes in overall brain growth rather than as a mechanism serving a specific behavioural adaptation.

Harsh and unpredictable environments and adverse internal states in childhood are each uniquely associated with fast life history behaviour: Aggression, impulsivity, and risk-taking in adolescence

External environment and internal state in relation to life-history behavioural profiles of adolescents in nine countries. Lei Chang et al. Proceedings of the Royal Society B, Volume 286, Issue 1917, December 18 2019. https://doi.org/10.1098/rspb.2019.2097

Abstract: The external environment has traditionally been considered as the primary driver of animal life history (LH). Recent research suggests that animals' internal state is also involved, especially in forming LH behavioural phenotypes. The present study investigated how these two factors interact in formulating LH in humans. Based on a longitudinal sample of 1223 adolescents in nine countries, the results show that harsh and unpredictable environments and adverse internal states in childhood are each uniquely associated with fast LH behavioural profiles consisting of aggression, impulsivity, and risk-taking in adolescence. The external environment and internal state each strengthened the LH association of the other, but overall the external environment was more predictive of LH than was the internal state. These findings suggest that individuals rely on a multitude and consistency of sensory information in more decisively calibrating LH and behavioural strategies.

4. Discussion

Existing research has shown, in separate studies, that both external environments and internal body states affect animal LH. Investigating these two factors in the same individuals, recent studies have demonstrated unique LH predictions by the two predictors (e.g. [33]). Findings of the present study add to the literature by showing the two factors interact in reinforcing LH calibration in the same direction. Childhood harsh and unpredictable environments and adverse internal states were each uniquely associated with fast LH behavioural profiles in adolescence, and each factor strengthened the LH association of the other factor. Specifically, at higher, compared to lower, levels of internal adversity, external harshness and unpredictability was more predictive of fast LH. Similarly, adverse internal state was predictive of fast LH when the external environment was harsh and unpredictable but not when it was benign. These conditional predictions suggest that external environments and internal body states likely reinforce the same cues about mortality–morbidity in accelerating fast LH. In the present study, we obtained information about childhood environmental harshness and unpredictability and adverse internal state at approximately the same time, 3 years before measuring LH profiles, therefore establishing longitudinal, unconditional, and conditional associations with or predictions of LH from the external and internal predictors. Additionally, external environment was more strongly associated with fast LH than was internal state as evidenced both by the two main effects (β = 0.50 versus 0.15) and the four conditional associations (figure 2). External environment may be an underlying cause of both fast LH behavioural profiles and internal body states [1] and, when this common variance was statistically accounted for in the present study by integrating the mediation modelling of the relation of external environment to internal state, LH prediction by the internal but not the external predictor was attenuated. These comprehensive findings support the conclusion that external environment has a stronger impact in shaping LH than internal state. Nonetheless, the internal state is still predictive of a fast LH behavioural profile overall and when external harshness and unpredictability are severe rather than benign.

Traditional LH theory emphasizes the environment as the sole actor in activating and formulating animal LH. Specifically, the mortality-causing harshness and unpredictability, as well as resource conditions (which were not investigated in the present study and have rarely been studied by other human LH research [8]), cause physiological (e.g. endocrine and homeostasis) and psychological tuning (e.g. cognitive and behaviour) that is oriented either towards growth and development (slow LH) or mating and reproduction (fast LH). Recent research has introduced animal internal state as a complementary actor in forming LH strategies [13,22,67]. In the light of the present findings, external environment and internal body state should not be distinguished as categorically separate drivers of LH. The two can be regarded as representing different and unique sensory inputs. For humans, the external environment is sensorially processed mainly as visual, auditory, and tactile data, whereas internal state is processed mainly as interoceptive including visceroceptive information. Humans and other animals processing more and more consistent sensory information should calibrate LH more decisively than those having less or less consistent information. Such is the implication of the present findings about the significant ordinal interaction effect. In the human case, for example, a child who constantly feels pains in her stomach while witnessing adult neighbours falling ill to a strange parasite should be more readily set on a faster LH path compared to the one who receives only one but not both sensory inputs or who receives two inconsistent inputs by experiencing external mortality but internal homeostasis or vice-versa.

A proviso to the present findings and discussion is that, like most of the existing human LH literature (e.g. [68]), the external environment operationalized in the present study was mostly individually specific, representing a person's unique home and family environment rather than a larger ecology shared with other conspecifics and thus increasing seeming consistency between external and internal conditions in impacting LH. This is not necessarily a limitation of the present study but, rather, represents the reality of LH research on contemporary human participants. Because humans have long mastered the external environment [69], most ecology-wide variables, such as mortality, pandemic and even intraspecific conflict that are traditionally defined in the species-general LH literature as extrinsic risks beyond individuals' survival effort, operate exactly depending on modern human individuals’ survival abilities or, more precisely, resource conditions. Thus, they do not fully satisfy the definition of extrinsic risks [70]. Because of these difficulties, individual-level variables, such as chaos at home, family misfunctioning, and unpredictable life events, have been substituted as proxies of extrinsic risks in human LH research (e.g. [40]). Another related weakness is using multi-informant reporting to measure internal states, as well as external environments, because individual differences in interoception may potentially be correlated with LH (e.g. [71]) and may in general confound the effects of body conditions. However, cognitive assessment of both internal and external information may become integral parts of human LH calibration. An appreciation of these human-specific conditions is needed in applying species-general models to study human LH. The present study represents such an appreciation and one of the first attempts to our knowledge to investigate how external environments and internal states interact in calibrating human LH behavioural profiles.