Quantifying maternal investment in mammals using allometry.

Maternal investment influences the survival and reproduction of both mothers and their progeny and plays a crucial role in understanding individuals' life-history and population ecology. To reveal the complex mechanisms associated with reproduction and investment, it is necessary to examine variations in maternal investment across species. Comparisons across species call for a standardised method to quantify maternal investment, which remained to be developed. This paper addresses this limitation by introducing the maternal investment metric - MI - for mammalian species, established through the allometric scaling of the litter mass at weaning age by the adult mass and investment duration (i.e. gestation + lactation duration) of a species. Using a database encompassing hundreds of mammalian species, we show that the metric is not highly sensitive to the regression method used to fit the allometric relationship or to the proxy used for adult body mass. The comparison of the maternal investment metric between mammalian subclasses and orders reveals strong differences across taxa. For example, our metric confirms that Eutheria have a higher maternal investment than Metatheria. We discuss how further research could use the maternal investment metric as a valuable tool to understand variation in reproductive strategies.

Cassette recombination dynamics within chromosomal integrons are regulated by toxin-antitoxin systems.

Integrons are adaptive bacterial devices that rearrange promoter-less gene cassettes into variable ordered arrays under stress conditions, thereby sampling combinatorial phenotypic diversity. Chromosomal integrons often carry hundreds of silent gene cassettes, with integrase-mediated recombination leading to rampant DNA excision and integration, posing a potential threat to genome integrity. How this activity is regulated and controlled, particularly through selective pressures, to maintain such large cassette arrays is unknown. Here, we show a key role of promoter-containing toxin-antitoxin (TA) cassettes as systems that kill the cell when the overall cassette excision rate is too high. These results highlight the importance of TA cassettes regulating the cassette recombination dynamics and provide insight into the evolution and success of integrons in bacterial genomes.

Innate immunity: the bacterial connection.

Pathogens have fueled the diversification of intracellular defense strategies that collectively define cell-autonomous innate immunity. In bacteria, innate immunity is manifested by a broad arsenal of defense systems that provide protection against bacterial viruses, called phages. The complexity of the bacterial immune repertoire has only been realized recently and is now suggesting that innate immunity has commonalities across the tree of life: many components of eukaryotic innate immunity are found in bacteria where they protect against phages, including the cGAS-STING pathway, gasdermins, and viperins. Here, I summarize recent findings on the conservation of innate immune pathways between prokaryotes and eukaryotes and hypothesize that bacterial defense mechanisms can catalyze the discovery of novel molecular players of eukaryotic innate immunity.

A conserved family of immune effectors cleaves cellular ATP upon viral infection.

During viral infection, cells can deploy immune strategies that deprive viruses of molecules essential for their replication. Here, we report a family of immune effectors in bacteria that, upon phage infection, degrade cellular adenosine triphosphate (ATP) and deoxyadenosine triphosphate (dATP) by cleaving the N-glycosidic bond between the adenine and sugar moieties. These ATP nucleosidase effectors are widely distributed within multiple bacterial defense systems, including cyclic oligonucleotide-based antiviral signaling systems (CBASS), prokaryotic argonautes, and nucleotide-binding leucine-rich repeat (NLR)-like proteins, and we show that ATP and dATP degradation during infection halts phage propagation. By analyzing homologs of the immune ATP nucleosidase domain, we discover and characterize Detocs, a family of bacterial defense systems with a two-component phosphotransfer-signaling architecture. The immune ATP nucleosidase domain is also encoded within diverse eukaryotic proteins with immune-like architectures, and we show biochemically that eukaryotic homologs preserve the ATP nucleosidase activity. Our findings suggest that ATP and dATP degradation is a cell-autonomous innate immune strategy conserved across the tree of life.

The evolutionary success of regulated cell death in bacterial immunity.

Bacteria employ a complex arsenal of immune mechanisms to defend themselves against phages. Recent studies demonstrate that these immune mechanisms frequently involve regulated cell death in response to phage infection. By sacrificing infected cells, this strategy prevents the spread of phages within the surrounding population. In this review, we discuss the principles of regulated cell death in bacterial defense, and show that over 70% of sequenced prokaryotes employ this strategy as part of their defensive arsenals. We highlight the modularity of defense systems involving regulated cell death, explaining how shuffling between phage-sensing and cell-killing protein domains dominates their evolution. Some of these defense systems are the evolutionary ancestors of key components of eukaryotic immunity, highlighting their importance in shaping the evolutionary trajectory of immune systems across the tree of life.

Mandrill mothers associate with infants who look like their own offspring using phenotype matching.

Behavioral discrimination of kin is a key process structuring social relationships in animals. In this study, we provide evidence for discrimination towards non-kin by third-parties through a mechanism of phenotype matching. In mandrills, we recently demonstrated increased facial resemblance among paternally related juvenile and adult females indicating adaptive opportunities for paternal kin recognition. Here, we hypothesize that mandrill mothers use offspring's facial resemblance with other infants to guide offspring's social opportunities towards similar-looking ones. Using deep learning for face recognition in 80 wild mandrill infants, we first show that infants sired by the same father resemble each other the most, independently of their age, sex or maternal origin, extending previous results to the youngest age class. Using long-term behavioral observations on association patterns, and controlling for matrilineal origin, maternal relatedness and infant age and sex, we then show, as predicted, that mothers are spatially closer to infants that resemble their own offspring more, and that this maternal behavior leads to similar-looking infants being spatially associated. We then discuss the different scenarios explaining this result, arguing that an adaptive maternal behavior is a likely explanation. In support of this mechanism and using theoretical modeling, we finally describe a plausible evolutionary process whereby mothers gain fitness benefits by promoting nepotism among paternally related infants. This mechanism, that we call 'second-order kin selection', may extend beyond mother-infant interactions and has the potential to explain cooperative behaviors among non-kin in other social species, including humans.

Mothers with higher twinning propensity had lower fertility in pre-industrial Europe.

Historically, mothers producing twins gave birth, on average, more often than non-twinners. This observation has been interpreted as twinners having higher intrinsic fertility - a tendency to conceive easily irrespective of age and other factors - which has shaped both hypotheses about why twinning persists and varies across populations, and the design of medical studies on female fertility. Here we show in >20k pre-industrial European mothers that this interpretation results from an ecological fallacy: twinners had more births not due to higher intrinsic fertility, but because mothers that gave birth more accumulated more opportunities to produce twins. Controlling for variation in the exposure to the risk of twinning reveals that mothers with higher twinning propensity - a physiological predisposition to producing twins - had fewer births, and when twin mortality was high, fewer offspring reaching adulthood. Twinning rates may thus be driven by variation in its mortality costs, rather than variation in intrinsic fertility.

Phages and their satellites encode hotspots of antiviral systems.

Bacteria carry diverse genetic systems to defend against viral infection, some of which are found within prophages where they inhibit competing viruses. Phage satellites pose additional pressures on phages by hijacking key viral elements to their own benefit. Here, we show that E. coli P2-like phages and their parasitic P4-like satellites carry hotspots of genetic variation containing reservoirs of anti-phage systems. We validate the activity of diverse systems and describe PARIS, an abortive infection system triggered by a phage-encoded anti-restriction protein. Antiviral hotspots participate in inter-viral competition and shape dynamics between the bacterial host, P2-like phages, and P4-like satellites. Notably, the anti-phage activity of satellites can benefit the helper phage during competition with virulent phages, turning a parasitic relationship into a mutualistic one. Anti-phage hotspots are present across distant species and constitute a substantial source of systems that participate in the competition between mobile genetic elements.

A treasure trove of molecular scissors.

Ancestral RNA-guided nucleases greatly expand the toolbox for gene editing.

GSpace: an exact coalescence simulator of recombining genomes under isolation by distance.

MOTIVATION: Simulation-based inference can bypass the limitations of statistical methods based on analytical approximations, but software allowing simulation of structured population genetic data without the classical n-coalescent approximations (such as those following from assuming large population size) are scarce or slow. RESULTS: We present GSpace, a simulator for genomic data, based on a generation-by-generation coalescence algorithm taking into account small population size, recombination and isolation by distance. AVAILABILITY AND IMPLEMENTATION: Freely available at site web INRAe (http://www1.montpellier.inra.fr/CBGP/software/gspace/download.html).

Lipoprotein DolP supports proper folding of BamA in the bacterial outer membrane promoting fitness upon envelope stress.

In Proteobacteria, integral outer membrane proteins (OMPs) are crucial for the maintenance of the envelope permeability barrier to some antibiotics and detergents. In Enterobacteria, envelope stress caused by unfolded OMPs activates the sigmaE (σE) transcriptional response. σE upregulates OMP biogenesis factors, including the ß-barrel assembly machinery (BAM) that catalyses OMP folding. Here we report that DolP (formerly YraP), a σE-upregulated and poorly understood outer membrane lipoprotein, is crucial for fitness in cells that undergo envelope stress. We demonstrate that DolP interacts with the BAM complex by associating with outer membrane-assembled BamA. We provide evidence that DolP is important for proper folding of BamA that overaccumulates in the outer membrane, thus supporting OMP biogenesis and envelope integrity. Notably, mid-cell recruitment of DolP had been linked to regulation of septal peptidoglycan remodelling by an unknown mechanism. We now reveal that, during envelope stress, DolP loses its association with the mid-cell, thereby suggesting a mechanistic link between envelope stress caused by impaired OMP biogenesis and the regulation of a late step of cell division.

Sex-specific spatial variation in fitness in the highly dimorphic Leucadendron rubrum.

Sexual dimorphism in plants may emerge as a result of sex-specific selection on traits enhancing access to nutritive resources and/or to sexual partners. Here we investigated sex-specific differences in selection of sexually dimorphic traits and in the spatial distribution of effective fecundity (our fitness proxy) in a highly dimorphic dioecious wind-pollinated shrub, Leucadendron rubrum. In particular, we tested for the effect of density on male and female effective fecundity. We used spatial and genotypic data of parent and offspring cohorts to jointly estimate individual male and female effective fecundity on the one hand and pollen and seed dispersal kernels on the other hand. This methodology was adapted to the case of dioecious species. Explicitly modelling dispersal avoids the confounding effects of heterogeneous spatial distribution of mates and sampled seedlings on the estimation of effective fecundity. We also estimated selection gradients on plant traits while modelling sex-specific spatial autocorrelation in fecundity. Males exhibited spatial autocorrelation in effective fecundity at a smaller scale than females. A higher local density of plants was associated with lower effective fecundity in males but was not related to female effective fecundity. These results suggest sex-specific sensitivities to environmental heterogeneity in L. rubrum. Despite these sexual differences, we found directional selection for wider canopies and smaller leaves in both sexes, and no sexually antagonistic selection on strongly dimorphic traits in L. rubrum. Many empirical studies in animals similarly failed to detect sexually antagonistic selection in species expressing strong sexual dimorphism, and we discuss reasons explaining this common pattern.

The impact of genetic diversity on gene essentiality within the Escherichia coli species.

Bacteria from the same species can differ widely in their gene content. In Escherichia coli, the set of genes shared by all strains, known as the core genome, represents about half the number of genes present in any strain. Although recent advances in bacterial genomics have unravelled genes required for fitness in various experimental conditions, most studies have focused on single model strains. As a result, the impact of the species' genetic diversity on core processes of the bacterial cell remains largely under-investigated. Here, we have developed a CRISPR interference platform for high-throughput gene repression that is compatible with most E. coli isolates and closely related species. We have applied it to assess the importance of ~3,400 nearly ubiquitous genes in three growth conditions in 18 representative E. coli strains spanning most common phylogroups and lifestyles of the species. Our screens revealed extensive variations in gene essentiality between strains and conditions. Investigation of the genetic determinants for these variations highlighted the importance of epistatic interactions with mobile genetic elements. In particular, we have shown how prophage-encoded defence systems against phage infection can trigger the essentiality of persistent genes that are usually non-essential. This study provides broad insights into the evolvability of gene essentiality and argues for the importance of studying various isolates from the same species under diverse conditions.

CRISPR screens in the era of microbiomes.

Recent advances in genomics have uncovered the tremendous diversity and richness of microbial ecosystems. New functional genomics methods are now needed to probe gene function in high-throughput and provide mechanistic insights. Here, we review how the CRISPR toolbox can be used to inactivate, repress or overexpress genes in a sequence-specific manner and how this offers diverse attractive solutions to identify gene function in high-throughput. Developed both in eukaryotes and prokaryotes, CRISPR screening technologies have already provided meaningful insights in microbiology and host-pathogen interactions. In the era of microbiomes, the versatility and the functional diversity of CRISPR-derived tools has the potential to significantly improve our understanding of microbial communities and their interaction with the host.

When Do Individuals Maximize Their Inclusive Fitness?

Adaptation is often described in behavioral ecology as individuals maximizing their inclusive fitness. Under what conditions does this hold, and how does this relate to the gene-centered perspective of adaptation? We unify and extend the literature on these questions to class-structured populations. We demonstrate that the maximization (in the best-response sense) of class-specific inclusive fitness obtains in uninvadable population states (meaning that all deviating mutants become extinct). This defines a genuine actor-centered perspective on adaptation. But this inclusive fitness is assigned to all bearers of a mutant allele in a given class and depends on distributions of demographic and genetic contexts. These distributions, in turn, usually depend on events in previous generations and are thus not under individual control. This prevents, in general, envisioning individuals themselves as autonomous fitness maximizers, each with its own inclusive fitness. For weak selection, however, the dependence on earlier events can be neglected. We then show that each individual in each class appears to maximize its own inclusive fitness when all other individuals exhibit inclusive fitness-maximizing behavior. This defines a genuine individual-centered perspective of adaptation and justifies formally, as a first-order approximation, the long-heralded view of individuals appearing to maximize their own inclusive fitness.

Farming plant cooperation in crops.

Selection of the fittest can promote individual competitiveness but often results in the erosion of group performance. Recently, several authors revisited this idea in crop production and proposed new practices based on selection for cooperative phenotypes, i.e. phenotypes that increase crop yield through decreased competitiveness. These recommendations, however, remain difficult to evaluate without a formal description of crop evolutionary dynamics under different selection strategies. Here, we develop a theoretical framework to investigate the evolution of cooperation-related traits in crops, using plant height as a case study. Our model is tailored to realistic agricultural practices and shows that combining high plant density, high relatedness and selection among groups favours the evolution of shorter plants that maximize grain yield. Our model allows us to revisit past and current breeding practices in light of kin selection theory, and yields practical recommendations to increase cooperation among crops and promote sustainable agriculture.