Evolutionary Determinants of Nonseasonal Breeding in Wild Chacma Baboons.

AbstractAnimal reproductive phenology varies from strongly seasonal to nonseasonal, sometimes among closely related or sympatric species. While the extent of reproductive seasonality is often attributed to environmental seasonality, this fails to explain many cases of nonseasonal breeding in seasonal environments. We investigated the evolutionary determinants of nonseasonal breeding in a wild primate, the chacma baboon (Papio ursinus), living in a seasonal environment with high climatic unpredictability. We tested three hypotheses proposing that nonseasonal breeding has evolved in response to (1) climatic unpredictability, (2) reproductive competition between females favoring birth asynchrony, and (3) individual, rank-dependent variations in optimal reproductive timing. We found strong support for an effect of reproductive asynchrony modulated by rank: (i) birth synchrony is costly to subordinate females, lengthening their interbirth intervals; (ii) females alter their reproductive timings (fertility periods and conceptions) in relation to previous conceptions in the group; and (iii) the reported effect of birth synchrony on interbirth intervals weakens the intensity of reproductive seasonality at the population level. This study emphasizes the importance of sociality in mediating the evolution of reproductive phenology in group-living organisms, a result of broad significance for understanding key demographic parameters driving population responses to increasing climatic fluctuations.

Birth timing generates reproductive trade-offs in a non-seasonal breeding primate.

The evolutionary benefits of reproductive seasonality are often measured by a single-fitness component, namely offspring survival. Yet different fitness components may be maximized by different birth timings. This may generate fitness trade-offs that could be critical to understanding variation in reproductive timing across individuals, populations and species. Here, we use long-term demographic and behavioural data from wild chacma baboons (Papio ursinus) living in a seasonal environment to test the adaptive significance of seasonal variation in birth frequencies. We identify two distinct optimal birth timings in the annual cycle, located four-month apart, which maximize offspring survival or minimize maternal interbirth intervals (IBIs), by respectively matching the annual food peak with late or early weaning. Observed births are the most frequent between these optima, supporting an adaptive trade-off between current and future reproduction. Furthermore, infants born closer to the optimal timing favouring maternal IBIs (instead of offspring survival) throw more tantrums, a typical manifestation of mother-offspring conflict. Maternal trade-offs over birth timing, which extend into mother-offspring conflict after birth, may commonly occur in long-lived species where development from birth to independence spans multiple seasons. Our findings therefore open new avenues to understanding the evolution of breeding phenology in long-lived animals, including humans.

Evolutionary implications of heterochromatin and rDNA in chromosome number and genome size changes during dysploidy: A case study in Reichardia genus.

In this study we showed that constitutive heterochromatin, GC-rich DNA and rDNA are implicated in chromosomal rearrangements during the basic chromosome number changing (dysploidy) in Reichardia genus. This small Mediterranean genus comprises 8-10 species and presents three basic chromosome numbers (x = 9, 8 and 7). To assess genome evolution and differentiation processes, studies were conducted in a dysploid series of six species: R. dichotoma, R. macrophylla and R. albanica (2n = 18), R. tingitana and R. gaditana (2n = 16), and R. picroides (2n = 14). The molecular phylogeny reconstruction comprised three additional species (R. crystallina and R. ligulata, 2n = 16 and R. intermedia, 2n = 14). Our results indicate that the way of dysploidy is descending. During this process, a positive correlation was observed between chromosome number and genome size, rDNA loci number and pollen size, although only the correlation between chromosome number and genome size is still recovered significant once considering the phylogenetic effect. Fluorescent in situ hybridisation also evidenced changes in number, position and organisation of two rDNA families (35S and 5S), including the reduction of loci number and, consequently, reduction in the number of secondary constrictions and nuclear organising regions from three to one per diploid genome. The potential mechanisms of chromosomal and genome evolution, strongly implicating heterochromatin, are proposed and discussed, with particular consideration for Reichardia genus.

The Evolution of Mutual Mate Choice under Direct Benefits.

In nature, the intensity of mate choice (i.e., choosiness) is highly variable within and between sexes. Despite growing empirical evidence of male and/or mutual mate choice, theoretical investigations of the joint evolution of female and male choosiness are few. In addition, previous approaches have often assumed an absence of trade-off between the direct benefits per mating and the lower mating rate that results from being choosy. Here we model the joint evolution of female and male choosiness when it is solely ruled by this fundamental trade-off. We show that this trade-off can generate a diversity of stable combinations of choosiness. Mutual mate choice can evolve only if both females and males exhibit long latency after mating. Furthermore, we show that an increase in choosiness in one sex does not necessarily prevent the evolution of mutual mate choice; the outcome depends on details shaping the trade-off: the life history, the decision rule for mate choice, and how the fecundity of a pair is shaped by the quality of both individuals. Last, we discuss the power of the sensitivity of the relative searching time (i.e., of the proportion of a lifetime spent searching for mates) as a predictor of the joint evolution of choosiness.

Social learning and the replication process: an experimental investigation.

Human cultural traits typically result from a gradual process that has been described as analogous to biological evolution. This observation has led pioneering scholars to draw inspiration from population genetics to develop a rigorous and successful theoretical framework of cultural evolution. Social learning, the mechanism allowing information to be transmitted between individuals, has thus been described as a simple replication mechanism. Although useful, the extent to which this idealization appropriately describes the actual social learning events has not been carefully assessed. Here, we used a specifically developed computer task to evaluate (i) the extent to which social learning leads to the replication of an observed behaviour and (ii) the consequences it has for fitness landscape exploration. Our results show that social learning does not lead to a dichotomous choice between disregarding and replicating social information. Rather, it appeared that individuals combine and transform information coming from multiple sources to produce new solutions. As a consequence, landscape exploration was promoted by the use of social information. These results invite us to rethink the way social learning is commonly modelled and could question the validity of predictions coming from models considering this process as replicative.

How choosy should I be? The relative searching time predicts evolution of choosiness under direct sexual selection.

Most theoretical research in sexual selection has focused on indirect selection. However, empirical studies have not strongly supported indirect selection. A well-established finding is that direct benefits and costs exert a strong influence on the evolution of mate choice. We present an analytical model in which unilateral mate choice evolves solely by direct sexual selection on choosiness. We show this is sufficient to generate the evolution of all possible levels of choosiness, because of the fundamental trade-off between mating rate and mating benefits. We further identify the relative searching time (RST, i.e. the proportion of lifetime devoted to searching for mates) as a predictor of the effect of any variable affecting the mating rate on the evolution of choosiness. We show that the RST: (i) allows one to make predictions about the evolution of choosiness across a wide variety of mating systems; (ii) encompasses all alternative variables proposed thus far to explain the evolution of choosiness by direct sexual selection; and (iii) can be empirically used to infer qualitative differences in choosiness.

Experimental evidence for the influence of group size on cultural complexity.

The remarkable ecological and demographic success of humanity is largely attributed to our capacity for cumulative culture. The accumulation of beneficial cultural innovations across generations is puzzling because transmission events are generally imperfect, although there is large variance in fidelity. Events of perfect cultural transmission and innovations should be more frequent in a large population. As a consequence, a large population size may be a prerequisite for the evolution of cultural complexity, although anthropological studies have produced mixed results and empirical evidence is lacking. Here we use a dual-task computer game to show that cultural evolution strongly depends on population size, as players in larger groups maintained higher cultural complexity. We found that when group size increases, cultural knowledge is less deteriorated, improvements to existing cultural traits are more frequent, and cultural trait diversity is maintained more often. Our results demonstrate how changes in group size can generate both adaptive cultural evolution and maladaptive losses of culturally acquired skills. As humans live in habitats for which they are ill-suited without specific cultural adaptations, it suggests that, in our evolutionary past, group-size reduction may have exposed human societies to significant risks, including societal collapse.

Social learners require process information to outperform individual learners.

Humans exhibit a rich and complex material culture with no equivalent in animals. Also, social learning, a crucial requirement for culture, is particularly developed in humans and provides a means to accumulate knowledge over time and to develop advanced technologies. However, the type of social learning required for the evolution of this complex material culture is still debated. Here, using a complex and opaque virtual task, the efficiency of individual learning and two types of social learning (product-copying and process-copying) were compared. We found that (1) individuals from process-copying groups outperformed individuals from product-copying groups or individual learners, whereas access to product information was not a sufficient condition for providing an advantage to social learners compared to individual learners; (2) social learning did not seem to affect the exploration of the fitness landscape; (3) social learning led to strong within-group convergence and also to between-group convergence, and (4) individuals used widely variable social learning strategies. The implications of these results for cumulative culture evolution are discussed.

Biased mutational pattern and quasispecies hypothesis in H5N1 virus.

Like other RNA viruses, influenza viruses are subject to high mutation rates. Carrying segmented RNA genomes, their genetic variability is even higher. We aimed at analyzing the mutational events occurring during the infection of chickens by the Highly Pathogenic Avian Influenza (HPAI) H5N1 virus. We therefore studied the different sequences of two surface proteins, hemagglutinin (HA) and neuraminidase (NA), as well as two internal proteins, PB2 and NS. Three organs (lung, spleen, brain) were obtained from a chicken, experimentally infected with a lethal dose of HPAI H5N1 virus. Cloning these PCR fragments enabled us to investigate the mutations undergone by the virus after several replicative cycles. The first outcome is the presence of a strong mutational bias, resembling host-driven ADAR1 adenosine deamination, which is responsible for 81% of all mutations. Whereas the frequency of RNA dependent RNA polymerase-related mutations is compatible with the survival of the virus, the ADAR1-like activity usually strongly increases the mutation frequency into a level of "error catastrophe" in theory incompatible with virus survival. Nevertheless, the virus was successfully infective. HPAI H5N1 virus displayed traits in agreement with the quasispecies theory. The role of this quasispecies structure in successful infection and the superposition with the ADAR1-like response is discussed.

Gametophytic vs. sporophytic control of pollen aperture number: a generational conflict.

In flowering plants, the haploid phase is reduced to the pollen grain and embryo sac. These reproductive tissues (gametophytes) are actually distinct individuals that have a different genome from the plant (sporophyte), and are more or less independent. The morphology of pollen grains, particularly the openings permitting pollen tube germination (apertures), is crucial for determining the outcome of pollen competition. Many species of flowering plants simultaneously produce pollen grains with different aperture numbers in a single individual (heteromorphism). In this paper, we show that the heteromorphic pollen aperture pattern depends on the genetic control of pollen morphogenesis. This points out a conflict of interest between genes expressed in the sporophyte and genes expressed in the gametophyte. More generally, such a conflict should exist whenever heteromorphism is an ESS resulting from a bet-hedging strategy. For pollen aperture, heteromorphism has been observed in about 40% of angiosperm species, suggesting that conflicting situations are the rule. In this context, the sporo-gametophytic conflict could be one of the factors that led to the reduction of the haploid phase in plants.

From preferred to actual mate characteristics: the case of human body shape.

The way individuals pair to produce reproductive units is a major factor determining evolution. This process is complex because it is determined not only by individual mating preferences, but also by numerous other factors such as competition between mates. Consequently, preferred and actual characteristics of mates obtained should differ, but this has rarely been addressed. We simultaneously measured mating preferences for stature, body mass, and body mass index, and recorded corresponding actual partner's characteristics for 116 human couples from France. Results show that preferred and actual partner's characteristics differ for male judges, but not for females. In addition, while the correlation between all preferred and actual partner's characteristics appeared to be weak for female judges, it was strong for males: while men prefer women slimmer than their actual partner, those who prefer the slimmest women also have partners who are slimmer than average. This study therefore suggests that the influences of preferences on pair formation can be sex-specific. It also illustrates that this process can lead to unexpected results on the real influences of mating preferences: traits considered as highly influencing attractiveness do not necessarily have a strong influence on the actual pairing, the reverse being also possible.

Mate choice and human stature: homogamy as a unified framework for understanding mating preferences.

Assortative mating for human height has long attracted interest in evolutionary biology, and the phenomenon has been demonstrated in numerous human populations. It is often argued that mating preferences generate this pattern, but other processes can also induce trait correlations between mates. Here, we present a methodology tailored to quantify continuous preferences based on choice experiments between pairs of stimuli. In particular, it is possible to explore determinants of interindividual variations in preferences, such as the height of the chooser. We collected data from a sample of 200 individuals from France. Measurements obtained show that the perception of attractiveness depends on both the height of the stimuli and the stature of the individual who judged them. Therefore, this study demonstrates that homogamy is present at the level of preferences for both sexes. We also show that measurements of the function describing this homogamy are concordant with several distinct mating rules proposed in the literature. In addition, the quantitative approach introduced here fulfills metrics that can be used to compare groups of individuals. In particular, our results reveal an important disagreement between sexes regarding height preferences in the context of mutual mate choice. Finally, both women and men prefer individuals who are significantly taller than average. All major findings are confirmed by a reanalysis of previously published data.

Height and body mass influence on human body outlines: a quantitative approach using an elliptic Fourier analysis.

Many studies use representations of human body outlines to study how individual characteristics, such as height and body mass, affect perception of body shape. These typically involve reality-based stimuli (e.g., pictures) or manipulated stimuli (e.g., drawings). These two classes of stimuli have important drawbacks that limit result interpretations. Realistic stimuli vary in terms of traits that are correlated, which makes it impossible to assess the effect of a single trait independently. In addition, manipulated stimuli usually do not represent realistic morphologies. We describe and examine a method based on elliptic Fourier descriptors to automatically predict and represent body outlines for a given set of predicted variables (e.g., sex, height, and body mass). We first estimate whether these predictive variables are significantly related to human outlines. We find that height and body mass significantly influence body shape. Unlike height, the effect of body mass on shape differs between sexes. Then, we show that we can easily build a regression model that creates hypothetical outlines for an arbitrary set of covariates. These statistically computed outlines are quite realistic and may be used as stimuli in future studies.

Geographical and within-population variation in the globeflower-globeflower fly interaction: the costs and benefits of rearing pollinator's larvae.

Interspecific interactions can vary within and among populations and geographical locations, and this variation can influence the nature of the interaction (e.g. mutualistic versus antagonistic) and its evolutionary stability. Globeflowers are exclusively pollinated by flies whose larvae feed only on their seeds. Here we document geographical variability in costs and benefits in globeflowers in sustaining their pollinating flies throughout the range of this arctic-alpine European plant over several years. A total of 1,710 flower heads from 38 populations were analysed for their carpel, egg and seed contents. Individual and population analyses control for the confounding influences of variation in both: (1) population traits, such as fly density and egg distribution among flower heads; and (2) individuals traits, such as carpel and egg numbers per flower head. Despite considerable variation in ecological conditions and pollinator densities across populations, large proportions (range 33-58%) of seeds are released after predation, with a benefit-to-cost ratio of 3, indicating that the mutualism is stable over the whole globeflower geographical range. The stability of the mutualistic interaction relies on density-dependent competition among larvae co-developing in a flower head. This competition is revealed by a sharp decrease in the number of seeds eaten per larva with increasing larval number, and is intensified by non-uniform egg distribution among globeflowers within a population. Carpel number is highly variable across globeflowers (range 10-69), and flies lay more eggs in large flowers. Most plants within a population contribute to the rearing of pollinators, but some pay more than others. Large globeflowers lose more seed to pollinator larvae, but also release more seed than smaller plants. The apparent alignment of interests between fly and plant (positive relationship between numbers of seeds released and destroyed) is shown to hide a conflict of interest found when flower size is controlled for.

Geographic and within-population variation in the globeflower-globeflower fly interaction: the costs and benefits of rearing pollinators' larvae.

Interspecific interactions can vary within and among populations and geographic locations, and this variation can influence the nature of the interaction (e.g. mutualistic vs. antagonistic) and its evolutionary stability. Globeflowers are exclusively pollinated by flies, whose larvae feed only on their seeds. Here we document geographic variability in costs and benefits in globeflowers in sustaining their pollinating flies throughout the range of this arctic-alpine European plant over several years. A total of 1,710 flower heads from 38 populations were analysed for their carpel, egg and seed contents. Individual and population analyses control for the confounding influences of variation in both: (1) population traits, such as fly density and egg distribution among flower heads; and (2) individuals traits, such as carpel and egg numbers per flower head. Despite considerable variation in ecological conditions and pollinator densities across populations, large proportions (range 33-58%) of seeds were released after predation, with a benefit-to-cost ratio of 3, indicating that the mutualism is stable over the whole globeflower geographical range. The stability of the mutualistic interaction relies on density-dependent competition among larvae co-developing in a flower head. This competition is revealed by a sharp decrease in the number of seeds eaten per larva with increasing larval number, and is intensified by non-uniform egg distribution among globeflowers within a population. Carpel number is highly variable across globeflowers (range 10-69), and flies lay more eggs in large flowers. Most plants within a population contribute to the rearing of pollinators, but the costs are greater for some than for others. Large globeflowers lose more seed to pollinator larvae, but also release more seed than smaller plants. The apparent alignment of interests between fly and plants (positive relationship between numbers of seed released and destroyed) is shown to hide a conflict of interest found when flower size is controlled for.

History of the Crested Lark in the Mediterranean region as revealed by mtDNA sequences and morphology.

The Crested Lark has a very complex taxonomy, partly as a result of a strong variation in plumage ground color seemingly linked with environmental factors. However, large variations in body size and bill shape further complicate the situation in the Maghreb. In this paper, we first present a set of hypotheses to explain patterns of morphological variation around the Mediterranean Sea. A phylogeographical analysis covering all major biogeographical areas in the species' range is then performed to test these scenarios. Three mtDNA groups with distinct geographical distribution were identified. The randonii clade (= G. (c.) randonii) is endemic from central Maghreb and is phylogenetically basal relative to cristata and senegallensis. These two latter groups are much more widespread. The cristata clade is found in NW Morocco, throughout Europe and W Asia and in NE Africa, while senegallensis regroups the populations sampled in the Western Sub-Saharan Africa and in NE Maghreb (E Algeria, Tunisia). A combination of genetic and paleoenvironmental evidences supports a scenario of allopatric differentiation of these two lineages outside the Maghreb, with subsequent range expansion leading to their secondary presence in the Maghreb. However, the alternative hypothesis of differentiation in two, or even three separate Maghreb refuges cannot be completely dismissed with the present data. Interestingly, the Sahara desert and the Gibraltar Strait did not act as permanent barriers to dispersal in this species. In addition, the populations in the Maghreb are consistently longer-billed than their closest relatives, suggesting a role for natural selection or phenotypic plasticity.

Within-host evolution and virulence in microparasites.

An important aspect of microparasite biology is the fact that infections are populations of thousands of microbes. As any population, infections are hence subject to two main types of changes: demographic and evolutionary. Here we analyse the consequences of within-host evolutionary changes. We build an epidemiological model where infections are regularly invaded by locally favored mutations affecting various infectious traits (virulence, transmissibility and clearance). Our results are the following. In durable infections, where within-host evolution is an important matter, a drop of transmissibility is only slightly deleterious to the infection, while a reduction of infection lifespan is very costly. In consequence, locally favored mutations reducing transmissibility reach a larger frequency, or even the complete fixation, and the suboptimality accumulated in infections owing to within-host evolution affects more their transmission than their duration. Conversely, taking an infection at random and observing the events of within-host evolution, one is more likely to observe reductions of infection length than reductions of transmissibility, because the mutations affecting transmissibility are often already present in infections. We then discuss the interpretation of these results in terms of deleterious mutations, and we also emphasize that the management of within-host evolution could be used as a novel therapeutic approach to the treatment of infection.

The evolution of mutation rate in finite asexual populations.

In this article, we model analytically the evolution of mutation rate in asexual organisms. Three selective forces are present. First, everything else being equal, individuals with higher mutation rate have a larger fitness, thanks to the energy and time saved by not replicating DNA accurately. Second, as a flip side, the genome of these individuals is replicated with errors that may negatively affect fitness. Third, and conversely, replication errors have a potential benefit if beneficial mutations are to be generated. Our model describes the fate of modifiers of mutation rate under the three forces and allows us to predict the long-term evolutionary trajectory of mutation rate. We obtain three major results. First, in asexuals, the needs for both adaptation and genome preservation are not evolutionary forces that can stabilize mutation rate at an intermediate optimum. When adaptation has a significant role, it primarily destabilizes mutation rate and yields the emergence of strong-effect mutators. Second, in contrast to what is usually believed, the appearance of modifiers with large mutation rate is more likely when the fitness cost of each deleterious mutation is weak, because the cost of replication errors is then paid after a delay. Third, in small populations, and even if adaptations are needed, mutation rate is always blocked at the minimum attainable level, because the rate of adaptation is too slow to play a significant role. Only populations whose size is above a critical mass see their mutation rate affected by the need for adaptation.

Diversification of transmission modes and the evolution of mutualism.

In order for mutualism to evolve, some force must align the interests of the two interacting partners. Vertical transmission can fill this role, but it is still unknown whether mutualism can be stable when vertically transmitted symbionts can evolve toward horizontal transmission. In this article, we investigate how symbionts' transmission mode and virulence should evolve, depending on the relationship between these two traits. We show that pathogens that reduce their host's fecundity can have more complex evolutionary dynamics than those that increase mortality. In some cases, runaway evolution of virulence can drive the host population extinct. In most cases, evolutionary branching results in the differentiation of avirulent, vertically transmitted symbionts from virulent, contagious pathogens. The population of symbionts then becomes polymorphic, and because the least virulent symbionts are the most frequent, the average virulence of symbionts is much lower than it would be in a monomorphic population. When the link between transmission and virulence results from correlated mutational changes and not from fixed constraints, vertically transmitted symbionts do not simply lose virulence; they evolve toward mutualism. We show that the force that stabilizes mutualism in such situations is the competition for transmission between symbionts.