Is more always better when it comes to mating?

Fitness usually increases when a male mates with more females, but is the same true for females? A new meta-analysis in PLOS Biology shows that females, like males, tend to have a positive relationship between the number of mates and their reproductive output. But why?

Asymmetric arms races between predators and prey: a tug of war between the life-dinner principle and the rare-enemy principle.

Antagonistic co-evolution can be asymmetric, where one species lags behind another. Asymmetry in a predator-prey context is expressed by the 'life-dinner principle', a classic informal model predicting that prey should be in some sense ahead in this arms race, since prey are running for their lives, while predators lag as they only run for their dinner. The model has undergone surprisingly little theoretical scrutiny. We derive analytical models that show coevolutionary outcomes do not always align with the life-dinner principle. Our results show that other important asymmetries can easily reverse the outcome, especially the rare-enemy principle: predators are usually outnumbered by their prey, sometimes substantially (trophic asymmetry), which can make selection on prey relatively weak. We additionally show that the antagonists typically exhibit different evolutionary responses to a situation where both predator and prey start out as equally fast runners. Although predators sometimes become so efficient that attacks always succeed, attack success often reaches a stable intermediate value. We conclude that the life-dinner principle has some validity as a metaphor, but its effect is of an 'all else being equal' type, which is surprisingly easily overridden by other features of the evolutionary dynamics.

Epidemiological and clinical burden of Clostridioides difficile infections and recurrences between 2015 - 2019: the RECUR Germany study.

BACKGROUND: This real-world study assessed the epidemiology and clinical complications of Clostridioides difficile infections (CDIs) and recurrences (rCDIs) in hospital and community settings in Germany from 2015 - 2019. METHODS: An observational retrospective cohort study was conducted among adult patients diagnosed with CDI in hospital and community settings using statutory health insurance claims data from the BKK database. A cross-sectional approach was used to estimate the annual incidence rate of CDI and rCDI episodes per 100,000 insurants. Patients' demographic and clinical characteristics were described at the time of first CDI episode. Kaplan-Meier method was used to estimate the time to rCDIs and time to complications (colonic perforation, colectomy, loop ileostomy, toxic megacolon, ulcerative colitis, peritonitis, and sepsis). A Cox model was used to assess the risk of developing complications, with the number of rCDIs as a time-dependent covariate. RESULTS: A total of 15,402 CDI episodes were recorded among 11,884 patients. The overall incidence of CDI episodes declined by 38% from 2015 to 2019. Most patients (77%) were aged ≥ 65 years. Around 19% of CDI patients experienced at least one rCDI. The median time between index CDI episode to a rCDI was 20 days. The most frequent complication within 12-months of follow-up after the index CDI episode was sepsis (7.57%), followed by colectomy (3.20%). The rate of complications increased with the number of rCDIs. The risk of any complication increased by 31% with each subsequent rCDI (adjusted hazard ratio [HR]: 1.31, 95% confidence interval: 1.17;1.46). CONCLUSIONS: CDI remains a public health concern in Germany despite a decline in the incidence over recent years. A substantial proportion of CDI patients experience rCDIs, which increase the risk of severe clinical complications. The results highlight an increasing need of improved therapeutic management of CDI, particularly efforts to prevent rCDI.

Estimating excess mortality and economic burden of Clostridioides difficile infections and recurrences during 2015-2019: the RECUR Germany study.

BACKGROUND: Clostridioides difficile infections (CDIs) and recurrences (rCDIs) remain a major public health challenge due to substantial mortality and associated costs. This study aims to generate real-world evidence on the mortality and economic burden of CDI in Germany using claims data between 2015 and 2019. METHODS: A longitudinal and matched cohort study using retrospective data from Statutory Health Insurance (SHI) was conducted in Germany with the BKK database. Adults diagnosed with CDI in hospital and community settings between 2015 and 2018 were included in the study. Patients had a minimum follow-up of 12-months. All-cause mortality was described at 6-, 12-, and 24-months. Healthcare resource usage (HCRU) and associated costs were assessed at 12-months of follow-up. A cohort of non-CDI patients matched by demographic and clinical characteristics was used to assess excess mortality and incremental costs of HCRU. Up to three non-CDI patients were matched to each CDI patient. RESULTS: A total of 9,977 CDI patients were included in the longitudinal cohort. All-cause mortality was 32%, 39% and 48% at 6-, 12-, and 24-months, respectively, with minor variations by number of rCDIs. When comparing matched CDI (n = 5,618) and non-CDI patients (n = 16,845), CDI patients had an excess mortality of 2.17, 1.35, and 0.94 deaths per 100 patient-months, respectively. HCRU and associated costs were consistently higher in CDI patients compared to non-CDI patients and increased with recurrences. Total mean and median HCRU cost per patient during follow-up was €12,893.56 and €6,050 in CDI patients, respectively, with hospitalisations representing the highest proportion of costs. A total mean incremental cost per patient of €4,101 was estimated in CDI patients compared to non-CDI patients, increasing to €13,291 in patients with ≥ 3 rCDIs. CONCLUSIONS: In this real-world study conducted in Germany, CDI was associated with increased risk of death and substantial costs to health systems due to higher HCRU, especially hospitalisations. HCRU and associated costs were exacerbated by rCDIs.

Transmissible cancers and the evolution of sex under the Red Queen hypothesis.

The predominance of sexual reproduction in eukaryotes remains paradoxical in evolutionary theory. Of the hypotheses proposed to resolve this paradox, the 'Red Queen hypothesis' emphasises the potential of antagonistic interactions to cause fluctuating selection, which favours the evolution and maintenance of sex. Whereas empirical and theoretical developments have focused on host-parasite interactions, the premises of the Red Queen theory apply equally well to any type of antagonistic interactions. Recently, it has been suggested that early multicellular organisms with basic anticancer defences were presumably plagued by antagonistic interactions with transmissible cancers and that this could have played a pivotal role in the evolution of sex. Here, we dissect this argument using a population genetic model. One fundamental aspect distinguishing transmissible cancers from other parasites is the continual production of cancerous cell lines from hosts' own tissues. We show that this influx dampens fluctuating selection and therefore makes the evolution of sex more difficult than in standard Red Queen models. Although coevolutionary cycling can remain sufficient to select for sex under some parameter regions of our model, we show that the size of those regions shrinks once we account for epidemiological constraints. Altogether, our results suggest that horizontal transmission of cancerous cells is unlikely to cause fluctuating selection favouring sexual reproduction. Nonetheless, we confirm that vertical transmission of cancerous cells can promote the evolution of sex through a separate mechanism, known as similarity selection, that does not depend on coevolutionary fluctuations.

Habitat detection, habitat choice copying or mating benefits: What drives conspecific attraction in a nomadic songbird?

Conspecific attraction during habitat selection is common among animals, but the ultimate (i.e. fitness-related) reasons for this behaviour often remain enigmatic. We aimed to evaluate the following three hypotheses for conspecific attraction during the breeding season in male Wood Warblers (Phylloscopus sibilatrix): the habitat detection hypothesis, the habitat choice copying hypothesis and the female preference hypothesis. These hypotheses make different predictions with respect to the relative importance of social and nonsocial information during habitat assessment, and whether benefits accrue as a consequence of aggregation. We tested the above hypotheses using a combination of a 2-year playback experiment, spatial statistics and mate choice models. The habitat detection hypothesis was the most likely explanation for conspecific attraction and aggregation in male Wood Warblers, based on the following results: (1) males were attracted to conspecific song playbacks, but fine-scale habitat heterogeneity was the better predictor of spatial patterns in the density of settling males; (2) male pairing success did not increase, but instead slightly decreased, as connectivity with other males (i.e. the number and proximity of neighbouring males) increased. Our study highlights how consideration of the process by which animals detect and assess habitat, together with the potential fitness consequences of resulting aggregations, are important for understanding conspecific attraction and spatially clustered distributions.

Serotype Replacement after Introduction of 10-Valent and 13-Valent Pneumococcal Conjugate Vaccines in 10 Countries, Europe.

We evaluated invasive pneumococcal disease (IPD) during 8 years of infant pneumococcal conjugate vaccine (PCV) programs using 10-valent (PCV10) and 13-valent (PCV13) vaccines in 10 countries in Europe. IPD incidence declined during 2011-2014 but increased during 2015-2018 in all age groups. From the 7-valent PCV period to 2018, IPD incidence declined by 42% in children <5 years of age, 32% in persons 5-64 years of age, and 7% in persons >65 years of age; non-PCV13 serotype incidence increased by 111%, 63%, and 84%, respectively, for these groups. Trends were similar in countries using PCV13 or PCV10, despite different serotype distribution. In 2018, serotypes in the 15-valent and 20-valent PCVs represented one third of cases in children <5 years of age and two thirds of cases in persons >65 years of age. Non-PCV13 serotype increases reduced the overall effect of childhood PCV10/PCV13 programs on IPD. New vaccines providing broader serotype protection are needed.

Volatile social environments can favour investments in quality over quantity of social relationships.

Cooperation does not occur in a vacuum: interactions develop over time in social groups that undergo demographic changes. Intuition suggests that stable social environments favour developing few but strong reciprocal relationships (a 'focused' strategy), while volatile social environments favour the opposite: more but weaker social relationships (a 'diversifying' strategy). We model reciprocal investments under a quality-quantity trade-off for social relationships. We find that volatility, counterintuitively, can favour a focused strategy. This result becomes explicable through applying the theory of antagonistic pleiotropy, originally developed for senescence, to social life. Diversifying strategies show superior performance later in life, but with costs paid at young ages, while the social network is slowly being built. Under volatile environments, many individuals die before reaching sufficiently old ages to reap the benefits. Social strategies that do well early in life are then favoured: a focused strategy leads individuals to form their first few social bonds quickly and to make strong use of existing bonds. Our model highlights the importance of pleiotropy and population age structure for the evolution of cooperative strategies and other social traits, and shows that it is not sufficient to reflect on the fate of survivors only, when evaluating the benefits of social strategies.

Selfish migrants: How a meiotic driver is selected to increase dispersal.

Meiotic drivers are selfish genetic elements that manipulate meiosis to increase their transmission to the next generation to the detriment of the rest of the genome. One example is the t haplotype in house mice, which is a naturally occurring meiotic driver with deleterious traits-poor fitness in polyandrous matings and homozygote inviability or infertility-that prevent its fixation. Recently, we discovered and validated a novel effect of t in a long-term field study on free-living wild house mice and with experiments: t-carriers are more likely to disperse. Here, we ask what known traits of the t haplotype can select for a difference in dispersal between t-carriers and wildtype mice. To that end, we built individual-based models with dispersal loci on the t and the homologous wildtype chromosomes. We also allow for density-dependent expression of these loci. The t haplotype consistently evolves to increase the dispersal propensity of its carriers, particularly at high densities. By examining variants of the model that modify different costs caused by t, we show that the increase in dispersal is driven by the deleterious traits of t, disadvantage in polyandrous matings and lethal homozygosity or male sterility. Finally, we show that an increase in driver-carrier dispersal can evolve across a range of values in driver strength and disadvantages.

Disentangling Verbal Arguments: Intralocus Sexual Conflict in Haplodiploids.

AbstractIn haplodiploids, (1) alleles spend twice as many generations in females as in males, (2) males are never heterozygous and therefore express recessive alleles, and (3) males sire daughters but not sons. Intralocus sexual conflict therefore operates differently in haplodiploids than in diploids and shares strong similarities with loci on X (or Z) chromosomes. The common co-occurrence of all three features makes it difficult to pinpoint their respective roles. However, they do not always co-occur in nature, and missing cases can be additionally studied with hypothetical life cycles. We model sexually antagonistic alleles in eight different sex determination systems and find that arguments 1 and 2 promote invasion and fixation of female-beneficial and male-beneficial alleles, respectively; argument 2 also improves prospects for polymorphism. Argument 3 harms the invasion prospects of sexually antagonistic alleles (irrespective of which sex benefits) but promotes fixation should invasion nevertheless occur. Disentangling the features helps to evaluate the validity of previous verbal arguments and yields better-informed predictions about intralocus sexual conflict under different sex determination systems, including hitherto undiscovered ones.

The stagnation paradox: the ever-improving but (more or less) stationary population fitness.

Fisher's fundamental theorem states that natural selection improves mean fitness. Fitness, in turn, is often equated with population growth. This leads to an absurd prediction that life evolves to ever-faster growth rates, yet no one seriously claims generally slower population growth rates in the Triassic compared with the present day. I review here, using non-technical language, how fitness can improve yet stay constant (stagnation paradox), and why an unambiguous measure of population fitness does not exist. Subfields use different terminology for aspects of the paradox, referring to stasis, cryptic evolution or the difficulty of choosing an appropriate fitness measure; known resolutions likewise use diverse terms from environmental feedback to density dependence and 'evolutionary environmental deterioration'. The paradox vanishes when these concepts are understood, and adaptation can lead to declining reproductive output of a population when individuals can improve their fitness by exploiting conspecifics. This is particularly readily observable when males participate in a zero-sum game over paternity and population output depends more strongly on female than male fitness. Even so, the jury is still out regarding the effect of sexual conflict on population fitness. Finally, life-history theory and genetic studies of microevolutionary change could pay more attention to each other.

Sexual dimorphism driven by intersexual resource competition: Why is it rare, and where to look for it?

Sexes often differ more obviously in secondary sexual characteristics than in traits that appear naturally selected, despite conceivable benefits to intersexual niche partitioning. Genetic constraints may play a role in limiting sex-specific niche evolution; however, it is not clear why this limit should apply to naturally selected traits more than those under sexual selection; the latter routinely produces dimorphism. We ask whether ecological factors and/or features of the mating system limit dimorphism in resource use, or conversely, what conditions are the most permissible ones for sexual niche differences. The scale of mating competition and spatial variation in resource availability can help predict sexually dimorphic niches or the lack thereof. We investigate why and when dimorphism might fail to evolve even if genetic covariation between the sexes posed no constraint. Our analytical model incorporates the first aspect of spatial interactions (scale of mating competition). It is followed by simulations that explore broader conditions, including multiple resources with habitat heterogeneity, genetic correlations and non-Gaussian resource-use efficiency functions. We recover earlier known conditions for favourable conditions for the evolution of niche partitioning between sexes, such as narrow individual niche and low degrees of genetic constraint. We also show spatial considerations to alter this picture. Sexual niche divergence occurs more readily when local mating groups are small and different resources occur reliably across habitats. Polygyny (medium-sized or large mating groups) can diminish the prospects for dimorphism even if no genetic constraints are present. Habitat heterogeneity typically also disfavours niche dimorphism but can also lead to polymorphism within a sex, if it is beneficial to specialize to be very competitive in one habitat, even at a cost to performance in the other. Sexual conflict is usually used to explain dimorphic traits or behaviours. Our models highlight that introducing conflict (achieved by switching from monogamy to polygamy) can also be responsible for sexual monomorphism. Under monogamy, males benefit from specializing to consume other resources than what feeds the female best. Polygyny makes males disregard this female benefit, and both sexes compete for the most profitable resource, leading to overlapping niches.

Optimal germination timing in unpredictable environments: the importance of dormancy for both among- and within-season variation.

For organisms living in unpredictable environments, timing important life-history events is challenging. One way to deal with uncertainty is to spread the emergence of offspring across multiple years via dormancy. However, timing of emergence is not only important among years, but also within each growing season. Here, we study the evolutionary interactions between germination strategies that deal with among- and within-season uncertainty. We use a modelling approach that considers among-season dormancy and within-season germination phenology of annual plants as potentially independent traits and study their separate and joint evolution in a variable environment. We find that higher among-season dormancy selects for earlier germination within the growing season. Furthermore, our results indicate that more unpredictable natural environments can counter-intuitively select for less risk-spreading within the season. Furthermore, strong priority effects select for earlier within-season germination phenology which in turn increases the need for bet hedging through among-season dormancy.

When Synchrony Makes the Best of Both Worlds Even Better: How Well Do We Really Understand Facultative Sex?

Biological diversity abounds in potential study topics. Studies of model systems have their advantages, but reliance on a few well-understood cases may create false impressions of what biological phenomena are the norm. Here I focus on facultative sex, which is often hailed as offering the best of both worlds, in that rare sex offers benefits almost equal to obligate sex and avoids paying most of the demographic costs. How well do we understand when and why this form of sexual reproduction is expected to prevail? I show several gaps in the theoretical literature and, by contrasting asynchronous with synchronous sex, highlight the need to link sex theories to the theoretical underpinnings of bet hedging, on the one hand, and to mate limitation considerations, on the other. Condition-dependent sex and links between sex with dispersal or dormancy appear understudied. While simplifications are justifiable as a simple assumption structure enhances analytical tractability, much remains to be done to incorporate key features of real sex to the main theoretical edifice.

An analysis of mating biases in trees.

Assortative mating is a deviation from random mating based on phenotypic similarity. As it is much better studied in animals than in plants, we investigate for trees whether kinship of realized mating pairs deviates from what is expected from the set of potential mates and use this information to infer mating biases that may result from kin recognition and/or assortative mating. Our analysis covers 20 species of trees for which microsatellite data is available for adult populations (potential mates) as well as seed arrays. We test whether mean relatedness of observed mating pairs deviates from null expectations that only take pollen dispersal distances into account (estimated from the same data set). This allows the identification of elevated as well as reduced kinship among realized mating pairs, indicative of positive and negative assortative mating, respectively. The test is also able to distinguish elevated biparental inbreeding that occurs solely as a result of related pairs growing closer to each other from further assortativeness. Assortative mating in trees appears potentially common but not ubiquitous: nine data sets show mating bias with elevated inbreeding, nine do not deviate significantly from the null expectation, and two show mating bias with reduced inbreeding. While our data sets lack direct information on phenology, our investigation of the phenological literature for each species identifies flowering phenology as a potential driver of positive assortative mating (leading to elevated inbreeding) in trees. Since active kin recognition provides an alternative hypothesis for these patterns, we encourage further investigations on the processes and traits that influence mating patterns in trees.

Species coexist more easily if reinforcement is based on habitat preferences than on species recognition.

Maladaptive hybridization selects for prezygotic isolation, a process known as reinforcement. Reinforcement reduces gene flow and contributes to the final stage of speciation. Ecologically, however, coexistence of the incipient species is difficult if they initially use identical resources. Habitat segregation offers an alternative to species discrimination as a way to reduce gene flow: production of unfit hybrids is reduced if mate encounters become rare due to differing habitat choice. Using a modelling approach, we show that hybridization avoidance alone can select for habitat specialization, even if neither of the species is intrinsically better at using a specific niche. While habitat segregation and species discrimination both reduce the risk of producing unfit hybrids, these two isolation mechanisms differ from each other with respect to their effects on resource competition. Our model shows that, as a consequence of such differences, reinforcement evolves much more easily if hybridization is avoided based on habitat segregation than if the mechanism involves species recognition (mate choice traits). We also examine the outcomes when both isolation mechanisms evolve jointly. The establishment of one isolation mechanism a priori weakens selection for the other. However, an asymmetry persists here too. The net effect of habitat segregation on species discrimination was typically facilitative, but not vice versa. This asymmetry arises because habitat segregation, by enhancing coexistence, secures time for the subsequent evolution of species discrimination in a mate choice context (still relevant if habitat use is not perfectly segregated). Species discrimination does not have such a stabilizing effect on coexistence. Our results emphasize the importance of habitat segregation in reinforcement and offer a way to interpret findings where closely related taxa show similar performance on different resources or in different habitats. Studies of ecological generalization and specialization should therefore take into account that niche differences can be initiated and/or maintained by hybridization avoidance.

Effect of childhood pneumococcal conjugate vaccination on invasive disease in older adults of 10 European countries: implications for adult vaccination.

BACKGROUND: Pneumococcal conjugate vaccines (PCVs) have the potential to prevent pneumococcal disease through direct and indirect protection. This multicentre European study estimated the indirect effects of 5-year childhood PCV10 and/or PCV13 programmes on invasive pneumococcal disease (IPD) in older adults across 13 sites in 10 European countries, to support decision-making on pneumococcal vaccination policies. METHODS: For each site we calculated IPD incidence rate ratios (IRR) in people aged ≥65 years by serotype for each PCV10/13 year (2011-2015) compared with 2009 (pre-PCV10/13). We calculated pooled IRR and 95% CI using random-effects meta-analysis and PCV10/13 effect as (1 - IRR)*100. RESULTS: After five PCV10/13 years, the incidence of IPD caused by all types, PCV7 and additional PCV13 serotypes declined 9% (95% CI -4% to 19%), 77% (95% CI 67% to 84%) and 38% (95% CI 19% to 53%), respectively, while the incidence of non-PCV13 serotypes increased 63% (95% CI 39% to 91%). The incidence of serotypes included in PCV13 and not in PCV10 decreased 37% (95% CI 22% to 50%) in six PCV13 sites and increased by 50% (95% CI -8% to 146%) in the four sites using PCV10 (alone or with PCV13). In 2015, PCV13 serotypes represented 20-29% and 32-53% of IPD cases in PCV13 and PCV10 sites, respectively. CONCLUSION: Overall IPD incidence in older adults decreased moderately after five childhood PCV10/13 years in 13 European sites. Large declines in PCV10/13 serotype IPD, due to the indirect effect of childhood vaccination, were countered by increases in non-PCV13 IPD, but these declines varied according to the childhood vaccine used. Decision-making on pneumococcal vaccination for older adults must consider the indirect effects of childhood PCV programmes. Sustained monitoring of IPD epidemiology is imperative.

Male-only care and cuckoldry in black coucals: does parenting hamper sex life?

Providing parental care often reduces additional mating opportunities. Paternal care becomes easier to understand if trade-offs between mating and caring remain mild. The black coucal Centropus grillii combines male-only parental care with 50% of all broods containing young sired by another male. To understand how much caring for offspring reduces a male's chance to sire additional young in other males' nests, we matched the production of extra-pair young in each nest with the periods during which potential extra-pair sires were either caring for offspring themselves or when they had no own offspring to care for. We found that males which cared for a clutch were not fully excluded from the pool of competitors for siring young in other males' nests. Instead, the relative siring success showed a temporary dip. Males were approximately 17% less likely to sire young in other males' nests while they were incubating, about 48% less likely to do so while feeding nestlings, followed by 26% when feeding fledglings, compared to the success of males that currently did not care for offspring. These results suggest that real-life care situations by males may involve trade-off structures that differ from, and are less strict than those frequently employed in theoretical considerations of operational sex ratios, sex roles and parenting decisions.

Science policies: How should science funding be allocated? An evolutionary biologists' perspective.

In an ideal world, funding agencies could identify the best scientists and projects and provide them with the resources to undertake these projects. Most scientists would agree that in practice, how funding for scientific research is allocated is far from ideal and likely compromises research quality. We, nine evolutionary biologists from different countries and career stages, provide a comparative summary of our impressions on funding strategies for evolutionary biology across eleven different funding agencies. We also assess whether and how funding effectiveness might be improved. We focused this assessment on 14 elements within four broad categories: (a) topical shaping of science, (b) distribution of funds, (c) application and review procedures, and (d) incentives for mobility and diversity. These comparisons revealed striking among-country variation in those elements, including wide variation in funding rates, the effort and burden required for grant applications, and the extent of emphasis on societal relevance and individual mobility. We use these observations to provide constructive suggestions for the future and urge the need to further gather informed considerations from scientists on the effects of funding policies on science across countries and research fields.