Journal of Evolutionary Biology

doi: 10.1111/jeb.13852pmid: N/A

Schlicht, Emmi; Kempenaers, Bart

doi: 10.1111/jeb.14201pmid: 37438929

Across birds, male age is the most consistent predictor of extra‐pair siring success, yet little is known about age effects on paternity over the lifetime of individuals. Here, we use data from a 13‐year study of a population of blue tits (Cyanistes caeruleus) to investigate how extra‐pair siring success changes with age within individuals. Our results indicate that extra‐pair siring success does not continuously increase with male age. Instead, siring success was related to male age in a threshold fashion, whereby yearling males were less likely to gain paternity than older males. This effect was independent of the age of the social partner, but influenced by the age of the extra‐pair female: success of yearlings at siring extra‐pair young (EPY) with older females was even lower. Among males that sired at least one EPY, the number of extra‐pair mates and the proportion of EPY sired were unrelated to male age. We found no evidence for an influence of selective disappearance on extra‐pair reproduction. Senescence, if anything, only occurs at ages blue tits rarely reach. A literature review indicates that an effect of male age on extra‐pair siring success may be limited to the switch from yearling to older in many species. Thus, the generally observed age effect on male extra‐pair siring success may be linked to age class rather than continuous ageing. This suggests that lack of experience or not fully completed maturation are important drivers of age patterns in extra‐pair paternity.AbstractIn the blue tit, success at gaining paternity in nests of other males (extra‐pair paternity) is related to male age in a threshold fashion: yearlings are less successful than older males. Yearling males may be losing out in competition with older males due to incomplete maturation, a lack of experience, or a female preference for older males.

Recuerda, María; Palacios, Mercè; Frías, Oscar; Hobson, Keith; Nabholz, Benoit; Blanco, Guillermo; Milá, Borja

doi: 10.1111/jeb.14200pmid: 37485603

According to models of ecological speciation, adaptation to adjacent, contrasting habitat types can lead to population divergence given strong enough environment‐driven selection to counteract the homogenizing effect of gene flow. We tested this hypothesis in the common chaffinch (Fringilla coelebs) on the small island of La Palma, Canary Islands, where it occupies two markedly different habitats. Isotopic (δ13C, δ15N) analysis of feathers indicated that birds in the two habitats differed in ecosystem and/or diet, and analysis of phenotypic traits revealed significant differences in morphology and plumage colouration that are consistent with ecomorphological and ecogeographical predictions respectively. A genome‐wide survey of single‐nucleotide polymorphism revealed marked neutral structure that was consistent with geography and isolation by distance, suggesting low dispersal. In contrast, loci putatively under selection identified through genome‐wide association and genotype‐environment association analyses, revealed a marked adaptive divergence between birds in both habitats. Loci associated with phenotypic and environmental differences among habitats were distributed across the genome, as expected for polygenic traits involved in local adaptation. Our results suggest a strong role for habitat‐driven local adaptation in population divergence in the chaffinches of La Palma, a process that appears to be facilitated by a strong reduction in effective dispersal distances despite the birds' high dispersal capacity.AbstractWe study the process of local adaptation in the common chaffinch to two contrasting habitats on the island of La Palma, the humid laurel forest and the dry pine forest. We document habitat‐related phenotypic divergence, and using genome–environment association analysis on a small fraction of the genome, we detect adaptive genomic divergence at a small spatial scale associated with habitat type.

Tschol, Maximilian; Reid, Jane M.; Bocedi, Greta

doi: 10.1111/jeb.14202pmid: 37497848

Sexual selection on males is predicted to increase population fitness, and delay population extinction, when mating success negatively covaries with genetic load across individuals. However, such benefits of sexual selection could be counteracted by simultaneous increases in genome‐wide drift resulting from reduced effective population size caused by increased variance in fitness. Resulting fixation of deleterious mutations could be greatest in small populations, and when environmental variation in mating traits partially decouples sexual selection from underlying genetic variation. The net consequences of sexual selection for genetic load and population persistence are therefore likely to be context dependent, but such variation has not been examined. We use a genetically explicit individual‐based model to show that weak sexual selection can increase population persistence time compared to random mating. However, for stronger sexual selection such positive effects can be overturned by the detrimental effects of increased genome‐wide drift. Furthermore, the relative strengths of mutation‐purging and drift critically depend on the environmental variance in the male mating trait. Specifically, increasing environmental variance caused stronger sexual selection to elevate deleterious mutation fixation rate and mean selection coefficient, driving rapid accumulation of drift load and decreasing population persistence times. These results highlight an intricate balance between conflicting positive and negative consequences of sexual selection on genetic load, even in the absence of sexually antagonistic selection. They imply that environmental variances in key mating traits, and intrinsic genetic drift, should be properly factored into future theoretical and empirical studies of the evolution of population fitness under sexual selection.AbstractIs sexual selection beneficial for small populations when it also increases genetic drift? We show that environmental variance in key mating traits modulates the net consequences of sexual selection for genetic load and the persistence of small populations.

Lev, Avigayil; Pischedda, Alison

doi: 10.1111/jeb.14206pmid: 37534751

Theory predicts that the strength of male mate choice should vary depending on male quality when higher‐quality males receive greater fitness benefits from being choosy. This pattern extends to differences in male body size, with larger males often having stronger pre‐ and post‐copulatory preferences than smaller males. We sought to determine whether large males and small males differ in the strength (or direction) of their preference for large, high‐fecundity females using the fruit fly, Drosophila melanogaster. We measured male courtship preferences and mating duration to show that male body size had no impact on the strength of male mate choice; all males, regardless of their size, had equally strong preferences for large females. To understand the selective pressures shaping male mate choice in males of different sizes, we also measured the fitness benefits associated with preferring large females for both large and small males. Male body size did not affect the benefits that males received: large and small males were equally successful at mating with large females, received the same direct fitness benefits from mating with large females, and showed similar competitive fertilization success with large females. These findings provide insight into why the strength of male mate choice was not affected by male body size in this system. Our study highlights the importance of evaluating the benefits and costs of male mate choice across multiple males to predict when differences in male mate choice should occur.AbstractLarge and small males show equally strong courtship and mating preferences for large, high‐fecundity females in Drosophila melanogaster, likely because male body size did not affect the fitness benefits that males received from being choosy: large and small males were equally successful at mating with large females, received the same direct fitness benefits from mating with large females, and showed similar competitive fertilization success with large females.

Mitchell, Christopher; Wylde, Zachariah; Del Castillo, Enrique; Rapkin, James; House, Clarissa M.; Hunt, John

doi: 10.1111/jeb.14198pmid: 37534753

Although many theoretical models of male sexual trait evolution assume that sexual selection is countered by natural selection, direct empirical tests of this assumption are relatively uncommon. Cuticular hydrocarbons (CHCs) are known to play an important role not only in restricting evaporative water loss but also in sexual signalling in most terrestrial arthropods. Insects adjusting their CHC layer for optimal desiccation resistance is often thought to come at the expense of successful sexual attraction, suggesting that natural and sexual selection are in opposition for this trait. In this study, we sampled the CHCs of male black field crickets (Teleogryllus commodus) using solid‐phase microextraction and then either measured their evaporative water loss or mating success. We then used multivariate selection analysis to quantify the strength and form of natural and sexual selection targeting male CHCs. Both natural and sexual selection imposed significant linear and stabilizing selection on male CHCs, although for very different combinations. Natural selection largely favoured an increase in the total abundance of CHCs, especially those with a longer chain length. In contrast, mating success peaked at a lower total abundance of CHCs and declined as CHC abundance increased. However, mating success did improve with an increase in a number of specific CHC components that also increased evaporative water loss. Importantly, this resulted in the combination of male CHCs favoured by natural selection and sexual selection being strongly opposing. Our findings suggest that the balance between natural and sexual selection is likely to play an important role in the evolution of male CHCs in T. commodus and may help explain why CHCs are so divergent across populations and species.AbstractNatural selection (measured via evaporative water loss) and sexual selection (measured via mating success) acting on cuticular hydrocarbons are opposing in male black field crickets (Teleogryllus commodus). This opposing pattern of selection has important implications for how variation is maintained in this important chemical trait.

Korfmann, Kevin; Abu Awad, Diala; Tellier, Aurélien

doi: 10.1111/jeb.14204pmid: 37551039

Seed banking (or dormancy) is a widespread bet‐hedging strategy, generating a form of population overlap, which decreases the magnitude of genetic drift. The methodological complexity of integrating this trait implies it is ignored when developing tools to detect selective sweeps. But, as dormancy lengthens the ancestral recombination graph (ARG), increasing times to fixation, it can change the genomic signatures of selection. To detect genes under positive selection in seed banking species it is important to (1) determine whether the efficacy of selection is affected, and (2) predict the patterns of nucleotide diversity at and around positively selected alleles. We present the first tree sequence‐based simulation program integrating a weak seed bank to examine the dynamics and genomic footprints of beneficial alleles in a finite population. We find that seed banking does not affect the probability of fixation and confirm expectations of increased times to fixation. We also confirm earlier findings that, for strong selection, the times to fixation are not scaled by the inbreeding effective population size in the presence of seed banks, but are shorter than would be expected. As seed banking increases the effective recombination rate, footprints of sweeps appear narrower around the selected sites and due to the scaling of the ARG are detectable for longer periods of time. The developed simulation tool can be used to predict the footprints of selection and draw statistical inference of past evolutionary events in plants, invertebrates, or fungi with seed banks.AbstractDormancy and seed banking are ubiquitous life history traits in plants, invertebrates, and microbes. We develop a simulation tool to generate polymorphism data over full chromosomes for species undergoing weak dormancy under neutral (mutation, recombination) and selective processes. We demonstrate that seed banks affect the signatures of selection in the polymorphism data, and enhance the detectability of selective sweeps.

Yıldırım, Burçin; Vogl, Claus

doi: 10.1111/jeb.14205pmid: 37564008

Among eukaryotes, the major spliceosomal pathway is highly conserved. While long introns may contain additional regulatory sequences, the ones in short introns seem to be nearly exclusively related to splicing. Although these regulatory sequences involved in splicing are well‐characterized, little is known about their evolution. At the 3′ end of introns, the splice signal nearly universally contains the dimer AG, which consists of purines, and the polypyrimidine tract upstream of this 3′ splice signal is characterized by over‐representation of pyrimidines. If the over‐representation of pyrimidines in the polypyrimidine tract is also due to avoidance of a premature splicing signal, we hypothesize that AG should be the most under‐represented dimer. Through the use of DNA‐strand asymmetry patterns, we confirm this prediction in fruit flies of the genus Drosophila and by comparing the asymmetry patterns to a presumably neutrally evolving region, we quantify the selection strength acting on each motif. Moreover, our inference and simulation method revealed that the best explanation for the base composition evolution of the polypyrimidine tract is the joint action of purifying selection against a spurious 3′ splice signal and the selection for pyrimidines. Patterns of asymmetry in other eukaryotes indicate that avoidance of premature splicing similarly affects the nucleotide composition in their polypyrimidine tracts.AbstractThe base composition of the polypyrimidine tract of short introns in Drosophila is influenced by purifying selection against a spurious 3′ splice signal and selection for pyrimidines, as shown by analysis of asymmetry patterns and population genetic modelling. Similar patterns in other eukaryotes suggest a common mechanism of base composition evolution.

Archetti, Marco

doi: 10.1111/jeb.14209pmid: 37584223

The adaptive value of sexual reproduction is still debated in evolutionary theory. It has been proposed that the advantage of sexual reproduction over asexual reproduction is to promote genetic diversity, to prevent the accumulation of harmful mutations or to preserve heterozygosity. Since these hypothetical advantages depend on the type of asexual reproduction, understanding how selection affects the taxonomic distribution of each type could help us discriminate between existing hypotheses. Here, I argue that soft selection, competition among embryos or offspring in selection arenas prior to the hard selection of the adult phase, reduces loss of heterozygosity in certain types of asexual reproduction. Since loss of heterozygosity leads to the unmasking of recessive deleterious mutations in the progeny of asexual individuals, soft selection facilitates the evolution of these types of asexual reproduction. Using a population genetics model, I calculate how loss of heterozygosity affects fitness for different types of apomixis and automixis, and I show that soft selection significantly reduces loss of heterozygosity, hence increases fitness, in apomixis with suppression of the first meiotic division and in automixis with central fusion, the most common types of asexual reproduction. Therefore, if sexual reproduction evolved to preserve heterozygosity, soft selection should be associated with these types of asexual reproduction. I discuss the evidence for this prediction and how this and other observations on the distribution of different types of asexual reproduction in nature is consistent with the heterozygosity hypothesis.AbstractCompetition among offspring promotes the types of asexual reproduction that produce offspring with variation in loss of complementation.

Peters, Madeline A. E.; Mideo, Nicole; MacPherson, Ailene

doi: 10.1111/jeb.14207pmid: 37610056

As a corollary to the Red Queen hypothesis, host–parasite coevolution has been hypothesized to maintain genetic variation in both species. Recent theoretical work, however, suggests that reciprocal natural selection alone is insufficient to maintain variation at individual loci. As highlighted by our brief review of the theoretical literature, models of host–parasite coevolution often vary along multiple axes (e.g. inclusion of ecological feedbacks or abiotic selection mosaics), complicating a comprehensive understanding of the effects of interacting evolutionary processes on diversity. Here we develop a series of comparable models to explore the effect of interactions between spatial structures and antagonistic coevolution on genetic diversity. Using a matching alleles model in finite populations connected by migration, we find that, in contrast to panmictic populations, coevolution in a spatially structured environment can maintain genetic variation relative to neutral expectations with migration alone. These results demonstrate that geographic structure is essential for understanding the effect of coevolution on biological diversity.AbstractOverview of the six matching alleles models considered and their main results for the maintenance of host genetic diversity. Bolded text in the top half of the figure indicates results in which coevolution maintained diversity, either transiently (relative to neutrality) or in the long term. The bottom half of the figure highlights model features, including host–parasite coevolution, spatial set‐up and time scale. In the coevolutionary model, hosts and parasites undergo both extrinsic birth and death as well as death and subsequent birth resulting from successful infection. Geography is defined as one of three options: one patch, two patches with migration and island–mainland with migration. Time scale is either continuous or discrete, with models correspondingly specified as either Moran or Wright–Fisher models.