Major Selective Force Research Articles

How should we measure population-level inbreeding depression? Impacts of standing genetic associations between selfing rate and deleterious mutations.

Inbreeding depression (ID) is a major selective force during mating system evolution primarily contributed by highly to partially recessive deleterious mutations. Theories suggest that transient genetic association with fitness alleles can be important in affecting the evolution of alleles that modify the selfing rate during its sweep. Nevertheless, empirical tests often focus on the pre-existing genetic association between selfing rate and ID maintained under mutation-selection balance. Therefore, how this standing genetic association is affected by key factors and its impacts on the evolution of selfing remain unclear. I show that as the selection coefficient of deleterious mutations increases, the association between selfing rate and ID declines from positive to negative. These results predict that association between selfing and ID tends to be negative in populations with low selfing rates, while positive in highly selfing populations. Using population genetic and quantitative genetic models, I show that standing genetic associations between selfing rate and fitness alleles can significantly impact the evolution of the mean selfing rate of a population. I present better metrics of population-level ID, which can be calculated based on the correlation coefficient between individual selfing rate and the fitness of selfed and outcrossed offspring.

Population-specific responses to pollution exposure suggest local adaptation of invasive red swamp crayfish Procambarus clarkii along the Mediterranean French coastline

Anthropogenic stressors can have an impact in a broad range of physiological processes and can be a major selective force leading to rapid evolution and local population adaptation. In this study, three populations of the invasive crayfish Procambarus clarkii were investigated. They are geographically separated for at least 20 years, and live in different abiotic environments: a freshwater inland lake (Salagou lake) with no major anthropogenic influence and two other coastal wetlands regularly polluted by pesticides along the Mediterranean coast (Camargue region and Bages-Sigean lagoon). Collected adults were genetically characterized using the mitochondrial COI gene and haplotype frequencies were analyzed for genetic variability within and between populations. Results revealed a higher genetic diversity for these invasive populations than any previous report in France, with more than seven different haplotypes in a single population. The contrasting genetic diversity between the Camargue and the other two populations suggest different times and sources of introduction. To identify differences in key physiological responses between these populations, individuals from each population were maintained in controlled conditions. Data on oxygen consumption rates indicate that the Salagou and Bages-Sigean populations possess a high inter-individual variability compared to the Camargue population. The low individual variability of oxygen consumption and low genetic diversity suggest a specific local adaptation for the Camargue population. Population-specific responses were identified when individuals were exposed to a pesticide cocktail containing azoxystrobin and oxadiazon at sublethal concentrations. The Salagou population was the only one with altered hydro-osmotic balance due to pollutant exposure and a change in protease activity in the hepatopancreas. These results revealed different phenotypic responses suggesting local adaptations at the population level.

Blocking then stinging as a case of two-step evolution of defensive cage architectures in herbivore-driven ecosystems.

Dense branching and spines are common features of plant species in ecosystems with high mammalian herbivory pressure. While dense branching and spines can inhibit herbivory independently, when combined, they form a powerful defensive cage architecture. However, how cage architecture evolved under mammalian pressure has remained unexplored. Here we show how dense branching and spines emerged during the age of mammalian radiation in the Combretaceae family and diversified in herbivore-driven ecosystems in the tropics. Phylogenetic comparative methods revealed that modern plant architectural strategies defending against large mammals evolved via a stepwise process. First, dense branching emerged under intermediate herbivory pressure, followed by the acquisition of spines that supported higher speciation rates under high herbivory pressure. Our study highlights the adaptive value of dense branching as part of a herbivore defence strategy and identifies large mammal herbivory as a major selective force shaping the whole plant architecture of woody plants.

Evolution of intermediate latency strategies in seasonal parasites.

Traditional mechanistic trade-offs between transmission and parasite latency period length are foundational for nearly all theories on the evolution of parasite life-history strategies. Prior theoretical studies demonstrate that seasonal host activity can generate a trade-off for obligate-host killer parasites that selects for intermediate latency periods in the absence of a mechanistic trade-off between transmission and latency period lengths. Extensions of these studies predict that host seasonal patterns can lead to evolutionary bistability for obligate-host killer parasites in which two evolutionarily stable strategies, a shorter and longer latency period, are possible. Here we demonstrate that these conclusions from previously published studies hold for non-obligate host killer parasites. That is, seasonal host activity can select for intermediate parasite latency periods for non-obligate killer parasites in the absence of a trade-off between transmission and latency period length and can maintain multiple evolutionarily stable parasite life-history strategies. These results reinforce the hypothesis that host seasonal activity can act as a major selective force on parasite life-history evolution by extending the narrower prior theory to encompass a greater range of disease systems.

Impact of dilution on stochastically driven methanogenic microbial communities of hypersaline anoxic sediments.

Sediments underlying the solar salterns of S'Avall are anoxic hypersaline ecosystems dominated by anaerobic prokaryotes, and with the especial relevance of putative methanogenic archaea. Slurries from salt-saturated sediments, diluted in a gradient of salinity and incubated for > 4 years revealed that salt concentration was the major selection force that deterministically structured microbial communities. The dominant archaea in the original communities showed a decrease in alpha diversity with dilution accompanied by the increase of bacterial alpha diversity, being highest at 5% salts. Correspondingly, methanogens decreased and in turn sulfate reducers increased with decreasing salt concentrations. Methanogens especially dominated at 25%. Different concentrations of litter of Posidonia oceanica seagrass added as a carbon substrate, did not promote any clear relevant effect. However, the addition of ampicillin as selection pressure exerted important effects on the assemblage probably due to the removal of competitors or enhancers. The amended antibiotic enhanced methanogenesis in the concentrations ≤ 15% of salts, whereas it was depleted at salinities ≥ 20% revealing key roles of ampicillin-sensitive bacteria.

A distinct Acyl-CoA binding protein (ACBP6) shapes tissue plasticity during nutrient adaptation in Drosophila

Nutrient availability is a major selective force in the evolution of metazoa, and thus plasticity in tissue function and morphology is shaped by adaptive responses to nutrient changes. Utilizing Drosophila, we reveal that distinct calibration of acyl-CoA metabolism, mediated by Acbp6 (Acyl-CoA binding-protein 6), is critical for nutrient-dependent tissue plasticity. Drosophila Acbp6, which arose by evolutionary duplication and binds acyl-CoA to tune acetyl-CoA metabolism, is required for intestinal resizing after nutrient deprivation through activating intestinal stem cell proliferation from quiescence. Disruption of acyl-CoA metabolism by Acbp6 attenuation drives aberrant ‘switching’ of metabolic networks in intestinal enterocytes during nutrient adaptation, impairing acetyl-CoA metabolism and acetylation amid intestinal resizing. We also identified STAT92e, whose function is influenced by acetyl-CoA levels, as a key regulator of acyl-CoA and nutrient-dependent changes in stem cell activation. These findings define a regulatory mechanism, shaped by acyl-CoA metabolism, that adjusts proliferative homeostasis to coordinately regulate tissue plasticity during nutrient adaptation.

Defensive responses: behaviour, the brain and the body.

Most animals live under constant threat from predators, and predation has been a major selective force inshaping animal behaviour. Nevertheless, defence responses against predatory threats need to be balanced against other adaptive behaviours such as foraging, mating and recovering from infection. This behavioural balance in ethologically relevant contexts requires adequate integration of internal and external signals in a complex interplay between the brain and the body. Despite this complexity, research has often considered defensive behaviour as entirely mediated by the brain processing threat-related information obtained via perception of the external environment. However, accumulating evidence suggests that theendocrine, immune, gastrointestinal and reproductive systems have important roles in modulating behavioural responses to threat. In this Review, we focus on how predatory threat defence responses are shaped by threat imminence and review the circuitry between subcortical brain regions involved in mediating defensive behaviours. Then, we discuss the intersection of peripheral systems involved in internal states related to infection, hunger and mating with the neurocircuits that underlie defence responses against predatory threat. Through this process, we aim to elucidate the interconnections between the brain and body as an integrated network that facilitates appropriate defensive responses to threat and todiscuss the implications for future behavioural research.

Inter-group alliance dynamics in Indo-Pacific bottlenose dolphins (Tursiops aduncus).

The social intelligence hypothesis holds that complex social relationships are the major selective force underlying the evolution of large brain size and intelligence. Complex social relationships are exemplified by coalitions and alliances that are mediated by affiliative behavior, resulting in differentiated but shifting relationships. Male Indo-Pacific bottlenose dolphins in Shark Bay, Australia, form three alliance levels or 'orders', primarily among non-relatives. Strategic alliance formation has been documented within both first- and second-order alliances and between second-order alliances ('third-order alliances'), revealing that the formation of strategic inter-group alliances is not limited to humans. Here we conducted a fine-scale study on 22 adult males over a 6-year period to determine if third-order alliance relationships are differentiated, and mediated by affiliative interactions. We found third-order alliance relationships were strongly differentiated, with key individuals playing a disproportionate role in maintaining alliances. Nonetheless, affiliative interactions occurred broadly between third-order allies, indicating males maintain bonds with third-order allies of varying strength. We also documented a shift in relationships and formation of a new third-order alliance. These findings further our understanding of dolphin alliance dynamics and provide evidence that strategic alliance formation is found in all three alliance levels, a phenomenon with no peer among non-human animals.

Cumulative early-life adversity does not predict reduced adult longevity in wild gorillas

Extensive research across fields has repeatedly confirmed that early-life adversity (ELA) is a major selective force for many taxa, in part via its ties to adult health and longevity.1,2,3 Negative effects of ELA on adult outcomes have been documented in a wide range of species, from fish to birds to humans.4 We used 55 years of long-term data collected on 253 wild mountain gorillas to examine the effects of six putative sources of ELA on survival, both individually and cumulatively. Although cumulative ELA was associated with high mortality in early life, we found no evidence that it had detrimental consequences for survival later in life. Experiencing three or more forms of ELA was associated with greater longevity, with a 70% reduction in the risk of death across adulthood, driven specifically by greater longevity in males. Although this higher survival in later life is likely a consequence of sex-specific viability selection5 during early life due to the immediate mortality consequences of adverse experiences, patterns in our data also suggest that gorillas have significant resilience to ELA. Our findings demonstrate that the detrimental consequences of ELA on later life survival are not universal, and indeed largely absent in one of humans' closest living relatives. This raises important questions about the biological roots of sensitivity to early experiences and the protective mechanisms that contribute to resiliency in gorillas, which could be critical for understanding how best to encourage similar resiliency to early-life shocks in humans.

Repeated colonization of alpine habitats by Arabidopsis arenosa viewed through freezing resistance and ice management strategies.

Success or failure of plants to cope with freezing temperatures can critically influence plant distribution and adaptation to new habitats. Especially in alpine environments, frost is a likely major selective force driving adaptation. In Arabidopsis arenosa (L.) Lawalrée, alpine populations have evolved independently in different mountain ranges, enabling studying mechanisms of acclimation and adaptation to alpine environments. We tested for heritable, parallel differentiation in freezing resistance, cold acclimation potential and ice management strategies using eight alpine and eight foothill populations. Plants from three European mountain ranges (Niedere Tauern, Făgăraș and Tatra Mountains) were grown from seeds of tetraploid populations in four common gardens, together with diploid populations from the Tatra Mountains. Freezing resistance was assessed using controlled freezing treatments and measuring effective quantum yield of photosystem II, and ice management strategies by infrared video thermography and cryomicroscopy. The alpine ecotype had a higher cold acclimation potential than the foothill ecotype, whereby this differentiation was more pronounced in tetraploid than diploid populations. However, no ecotypic differentiation was found in one region (Făgăraș), where the ancient lineage had a different evolutionary history. Upon freezing, an ice lens within a lacuna between the palisade and spongy parenchyma tissues was formed by separation of leaf tissues, a mechanism not previously reported for herbaceous species. The dynamic adjustment of freezing resistance to temperature conditions may be particularly important in alpine environments characterized by large temperature fluctuations. Furthermore, the formation of an extracellular ice lens may be a useful strategy to avoid tissue damage during freezing.

A fungus infected environment does not alter the behaviour of foraging ants

Eusocial insects are exposed to a wide range of pathogens while foraging outside their nest. We know that opportunistic scavenging ants are able to assess the sanitary state of food and to discriminate a prey which died from infection by the entomopathogenic fungus Metarhizium brunneum. Here, we investigate whether a contamination of the environment can also influence the behaviour of foragers, both at the individual and collective level. In a Y-maze, Myrmica rubra ants had the choice to forage on two prey patches, one of which containing sporulating items. Unexpectedly, the nearby presence of sporulating bodies did not deter foragers nor prevent them from retrieving palatable prey. Ant colonies exploited both prey patches equally, without further mortality resulting from foraging on the contaminated area. Thus, a contamination of the environment did not prompt an active avoidance by foragers of which the activity depended primarily on the food characteristics. Generalist entomopathogenic fungi such as M. brunneum in the area around the nest appear more to be of a nuisance to ant foragers than a major selective force driving them to adopt avoidance strategies. We discuss the cost–benefit balance derived from the fine-tuning of strategies of pathogen avoidance in ants.

Evidence of nutrient translocation in response to smoke exposure by the East African ant acacia, Vachellia drepanolobium.

Fire is a major selective force on arid grassland communities, favoring traits such as the smoke‐induced seed germination response seen in a wide variety of plant species. However, little is known about the relevance of smoke as a cue for plants beyond the seedling stage.We exposed a fire‐adapted savanna tree, Vachellia (=Acacia) drepanolobium, to smoke and compared nutrient concentrations in leaf and root tissues to unexposed controls. Experiments were performed on three age cohorts: 2‐year‐old, 9‐month‐old, and 3‐month‐old plants.For the 2‐year‐old plants exposed to smoke, carbon and nitrogen concentrations were lower in the leaves and higher in the roots than controls. Less pronounced trends were found for boron and magnesium.In contrast, smoke‐exposed 3‐month‐old plants had lower root nitrogen concentrations than controls. No significant differences were found in the 9‐month‐old plants, and no significant shifts in other nutrient concentrations were observed between plant tissues for any of the three age cohorts. Synthesis: Our findings are consistent with smoke‐induced translocation of nutrients from leaves to roots in 2‐year‐old V. drepanolobium. This could represent a novel form of fire adaptation, with variation over the course of plant development. The translocation differences between age cohorts highlight the need to investigate smoke response in older plants of other species. Accounting for this adaptation could better inform our understanding of savanna community structure and nutrient flows under fire regimes altered by anthropogenic land use and climate change.

Rapid Evolutionary Adaptation in Response to Selection on Quantitative Traits.

Evolutionary adaptation after sudden environmental changes can occur very rapidly. The mechanisms facilitating rapid adaptation range from strong positive directional selection leading to large shifts in the allele frequencies at a few loci (selective sweeps) to polygenic selection causing small changes in allele frequencies at many loci. In addition, combinations of these two extreme mechanisms may also result in fast evolution. In recent years, following reports of new case studies of rapid adaptation, population genetic models have been proposed to explain these observations. In these models, the role of the major selective forces (positive directional and stabilizing selection) is highlighted as well as the genetic architecture of quantitative traits. Furthermore, the factors limiting the speed of adaptation are analyzed, in particular, the effects of random genetic drift and demography due to finite population size.

Experimental size- and sex-specific predation on dung flies by amphibian and arthropod predators

Abstract Because predator-prey interactions in nature are multifarious, linking phenomenological predation rates to underlying behavioral or ecological mechanisms is challenging. Size- and sex-specific predation has been implicated as a major selective force keeping animals small, directing the evolution of body size and sexual size dimorphism. We experimentally assessed predation by 4 amphibian and 3 arthropod species (bug, fly, spider) on 3 species of dung flies with similar ecology but contrasting body sizes, sexual size dimorphism, and coloration. Predators were offered a size range of male and/or female individuals of one prey species. As expected based on optimal foraging theory, some anurans (Bufo bufo) preferred larger prey individuals, others (Bombina variagata, Rana esculenta) showed no preference. Small juvenile Rana temporaria metamorphs preferred small prey, as did all arthropod predators, a pattern that may be explained by gape limitation or larger prey escaping better. Presumably more mobile males were not preyed upon more frequently or faster than cryptic females, even when conspicuously colored. Contrary to expectation, predation rates on flies in mixed groups facilitating mating activity were not higher, nor was predation generally sex-specific, hence contributing little to sexual dimorphism. We conclude that the size-selectivity of predators, and hence the viability selection pattern exerted on their prey, depends foremost on the relative body sizes of the two in a continuous fashion, in addition to any specific prey defense mechanisms. Therefore, the mechanistic study of predation requires integration of both the predator and prey perspectives, and phenomenological field studies of predation remain indispensable.

Is plant reproductive efficiency expressed on a continuum of facilitation and competition?

AbstractQuestionsCompetition and facilitation form a continuum of interactions between plants from intensely negative to intensely positive. Competition has long been understood to be a major selective force driving the expression of adaptive strategies in plants. However, we remain uncertain if facilitation plays a similar role. In previous studies, the relative allocation to reproduction across plant species increases with increasing competition intensity, and this observation is generally consistent with life history theory (rather than traditional plant strategy theory). However, is facilitation also an important force in shaping adaptive strategies in plants?MethodsWe surveyed the literature for plant facilitation studies that included measures of plant performance (e.g. vegetative biomass, height) and reproduction (e.g. reproductive biomass, seed number). We tested for a relationship between relative reproductive efficiency (the allocation to reproduction in the presence of neighbours relative to the allocation of reproduction in the absence of neighbours), and facilitation interaction intensity (i.e. the increase in plant performance due to the presence of neighbours). We also compared this relationship to the previously published relationship between reproductive efficiency and competition intensity to test for a continuum of strategies on an axis of plant–plant interactions from intensely positive (facilitation) to intensely negative (competition).ResultsThe overall relationship between facilitation intensity and the relative reproductive efficiency is a common negative relationship for both annual and perennial life histories. We found a highly significant negative relationship across the competition–facilitation continuum, with reproductive efficiency in the presence of neighbouring vegetation high under intense competition and low under intense facilitation.ConclusionPlant reproductive strategies are expressed on a continuum of interactions from facilitation to competition. This continuum of interactions will be important in understanding how interactions between plants drive the evolution of adaptive strategies and control coexistence and diversity in plant communities.

Testing Pollination Syndromes in <i>Oenothera</i> (Onagraceae)

Pollinators are considered a major selective force in shaping the diversification of angiosperms. It has been hypothesized that convergent evolution of floral form has resulted in “pollination syndromes” - i.e. suites of floral traits that correspond to attraction of particular pollinator functional groups. Across the literature, the pollination syndrome concept has received mixed support. This may be due to studies using different methods to describe floral traits and/or the pollination syndrome concept being supported more often in species highly reliant on pollinators for reproduction. Here, we assess the predictive ability of pollination syndromes in Oenothera, a species rich clade with pollination systems existing on a gradient of specialization, and in which species are either self-compatible or self-incompatible. We ask the following questions: Do Oenothera species follow the pollination syndrome concept using traditional, categorical floral trait descriptions and/or quantitative floral trait measurements? And, are floral traits more predictive of primary pollinators in species with specialized pollination systems and/or species that are self-incompatible? Mapping floral traits of 54 Oenothera species into morphospace, we do not find support for the pollination syndrome concept using either categorical or quantitative floral trait descriptions. We do not find support for specialization or breeding system influencing the prediction of primary pollinators. However, we find pollination syndromes were more predictive in Oenothera species with moth pollination systems. Collectively, these results suggest that the pollination syndrome concept cannot be generally applied across taxa and that evolutionary history is important to consider when evaluating the relationship between floral form and contemporary pollinators.

Radiology’s Information Architecture Could Migrate to One Emulating That of Smartphones

Diagnostic radiology (DxR), having had successful serial co-evolutions with imaging equipment and PACS, is faced with another. With a backdrop termed "globotics transition," it should create an IT and informatics infrastructure capable of integrating artificial intelligence (AI) into current critical communication functions of PACS and incorporating functions currently residing in balkanized products. DxR will face the challenge of adopting sustaining and disruptive AI innovations simultaneously. In this co-evolution, a major selection force for AI will be increasing the flow of information and patients; "increasing" means faster flow over larger areas defined by geography and content. Larger content includes a broader spectrum of imaging and nonimaging information streams that facilitate medical decision making. Evolution to faster flow will gravitate toward a hierarchical IT architecture consisting of many small channels feeding into fewer larger channels, something potentially difficult for current PACS. Smartphone-like architecture optimized for communication and integration could provide a large-channel backbone and many smaller feeding channels for basic functions, as well as those needing to innovate rapidly. New, more flexible architectures stimulate market competition in which DxR could act as an artificial selection force to influence development of faster increased flow in current PACS companies, in disruptors such as consolidated AI companies, or in entirely new entrants like Apple or Google. In this co-evolution, DxR should be able to stimulate design of a modern communication medium that increases the flow of information and decreases the time and energy necessary to absorb it, thereby creating even more indispensable clinical value for itself.

Differential Expression of Immune Genes between Two Closely Related Beetle Species with Different Immunocompetence following Attack by Asecodes parviclava.

Endoparasitoid wasps are important natural enemies of many insect species and are major selective forces on the host immune system. Despite increased interest in insect antiparasitoid immunity, there is sparse information on the evolutionary dynamics of biological pathways and gene regulation involved in host immune defense outside Drosophila species. We de novo assembled transcriptomes from two beetle species and used time-course differential expression analysis to investigate gene expression differences in closely related species Galerucella pusilla and G. calmariensis that are, respectively, resistant and susceptible against parasitoid infection by Asecodes parviclava parasitoids. Approximately 271 million and 224 million paired-ended reads were assembled and filtered to form 52,563 and 59,781 transcripts for G. pusilla and G. calmariensis, respectively. In the whole-transcriptome level, an enrichment of functional categories related to energy production, biosynthetic process, and metabolic process was exhibited in both species. The main difference between species appears to be immune response and wound healing process mounted by G. pusilla larvae. Using reciprocal BLAST against the Drosophila melanogaster proteome, 120 and 121 immune-related genes were identified in G. pusilla and G. calmariensis, respectively. More immune genes were differentially expressed in G. pusilla than in G. calmariensis, in particular genes involved in signaling, hematopoiesis, and melanization. In contrast, only one gene was differentially expressed in G. calmariensis. Our study characterizes important genes and pathways involved in different immune functions after parasitoid infection and supports the role of signaling and hematopoiesis genes as key players in host immunity in Galerucella against parasitoid wasps.

The fruitless gene affects female receptivity and species isolation.

Female mate rejection acts as a major selective force within species, and can serve as a reproductive barrier between species. In spite of its critical role in fitness and reproduction, surprisingly little is known about the genetic or neural basis of variation in female mate choice. Here, we identify fruitless as a gene affecting female receptivity within Drosophila melanogaster, as well as female Drosophila simulans rejection of male D. melanogaster. Of the multiple transcripts this gene produces, by far the most widely studied is the sex-specifically spliced transcript involved in the sex determination pathway. However, we find that female rejection behaviour is affected by a non-sex-specifically spliced fruitless transcript. This is the first implication of fruitless in female behaviour, and the first behavioural role identified for a fruitless non-sex-specifically spliced transcript. We found that this locus does not influence preferences via a single sensory modality, examining courtship song, antennal pheromone perception, or perception of substrate vibrations, and we conclude that fruitless influences mate choice via the integration of multiple signals or through another sensory modality.

Intergroup aggression in meerkats.

Violent conflicts between groups have been observed among many species of group living mammals and can have important fitness consequences, with individuals being injured or killed and with losing groups surrendering territory. Here, we explore between-group conflict among meerkats (Suricata suricatta), a highly social and cooperatively breeding mongoose. We show that interactions between meerkat groups are frequently aggressive and sometimes escalate to fighting and lethal violence and that these interactions have consequences for group territories, with losing groups moving to sleeping burrows closer to the centre of their territories following an intergroup interaction and with winning groups moving further away. We find that larger groups and groups with pups are significantly more likely to win contests, but that the location of the contest, adult sex ratio, and mean within-group genetic relatedness do not predict contest outcome. Our results suggest that intergroup competition may be a major selective force among meerkats, reinforcing the success of large groups and increasing the vulnerability of small groups to extinction. The presence of both within-group cooperation and between-group hostility in meerkats make them a valuable point of comparison in attempts to understand the ecological and evolutionary roots of human warfare.