Sequential polyandry affords post-mating sexual selection in the mouths of cichlid females

Females mating with multiple males may obtain direct benefits such as nuptial gifts or paternal care or indirect (i.e. genetic) benefits resulting in higher-quality offspring. While direct benefits are easily identified, it is difficult to determine indirect benefits, and it is hence largely unclear how they are obtained. This is particularly true in species with external fertilisation, where females seem to have little control over fertilisation. In cichlids, most maternal mouthbrooders show sequential multiple mating, where females visit several males for egg deposition. Genetic data revealed that multiple paternity of eggs and young in the mouth of females is common, but behavioural data of female spawning decisions are missing. Here, we test four hypotheses to explain female multiple mating in the maternally mouthbrooding cichlid, Ophthalmotilapia ventralis: (1) fertilisation insurance, (2) genetic bet-hedging, (3) female choice and (4) ‘sperm shopping' (i.e. induction of sperm competition resulting in sexually selected sperm). Detailed observations of spawning behaviour in the field combined with histological analyses of the male reproductive organs suggest that fertilisation insurance, genetic bet-hedging and pre-mating female choice are unlikely to explain the sequential female multiple mating in O. ventralis. Instead, cryptic female choice by sperm shopping, i.e. post-mating sexual selection, is most compatible with our data and might be the major ultimate cause of multiple mating in females of this species and of mouthbrooding cichlids with maternal care in general. Our study provides new insight into ultimate causes of sequential polyandry in species with external fertilisation, as hitherto post-mating sexual selection by cryptic female choice has been assumed to be incompatible with external fertilisation mechanisms except by components of the ovarian flui

Within-ejaculate sperm competition

Sperm competition was defined by Geoff Parker 50 years ago as the competition between sperm from two or more males over the fertilization of a set of eggs. Since the publication of his seminal paper, sperm competition has developed into a large field of research, and many aspects are still being discovered. One of the relatively poorly understood aspects is the importance of selection and competition among sperm within the ejaculate of a male. The sheer number of sperm present in a male's ejaculate suggests that the competition among sibling sperm produced by the same male may be intense. In this review, we summarize Parker's theoretical models generating predictions about the evolution of sperm traits under the control of the haploid gamete as opposed to the diploid male. We review the existing evidence of within-ejaculate competition from a wide range of fields and taxa. We also discuss the conceptual and practical hurdles we have been facing to study within-ejaculate sperm competition, and how novel technologies may help in addressing some of the currently open questions. This article is part of the theme issue 'Fifty years of sperm competition'

Trade-off between somatic and germline repair in a vertebrate supports the "expensive germ line" hypothesis

The disposable soma theory is a central tenet of the biology of aging where germline immortality comes at the cost of an aging soma [T. B. L. Kirkwood, Nature 270, 301–304 (1977); T. B. L. Kirkwood, Proc. R. Soc. Lond. B Biol. Sci. 205, 531–546 (1979); T. B. L. Kirkwood, S. N. Austad, Nature 408, 233–238 (2000)]. Limited resources and a possible trade-off between the repair and maintenance of the germ cells and growth and maintenance of the soma may explain the deterioration of the soma over time. Here we show that germline removal allows accelerated somatic healing under stress. We tested “the expensive germ line” hypothesis by generating germline-free zebrafish Danio rerio and testing the effect of the presence and absence of the germ line on somatic repair under benign and stressful conditions. We exposed male fish to sublethal low-dose ionizing radiation, a genotoxic stress affecting the soma and the germ line, and tested how fast the soma recovered following partial fin ablation. We found that somatic recovery from ablation occurred substantially faster in irradiated germline-free fish than in the control germline-carrying fish where somatic recovery was stunned. The germ line did show signs of postirradiation recovery in germline-carrying fish in several traits related to offspring number and fitness. These results support the theoretical conjecture that germline maintenance is costly and directly trades off with somatic maintenance

Haploid selection in "diploid" organisms

Evolutionary rates and strength of selection differ markedly between haploid and diploid genomes. Any genes expressed in a haploid state will be directly exposed to selection, whereas alleles in a diploid state may be partially or fully masked by a homologous allele. This difference may shape key evolutionary processes, including rates of adaptation and inbreeding depression, but also the evolution of sex chromosomes, heterochiasmy, and stable sex ratio biases. All diploid organisms carry haploid genomes, most notably the haploid genomes in gametes produced by every sexually reproducing eukaryote. Furthermore, haploid expression occurs in genes with monoallelic expression, in sex chromosomes, and in organelles, such as mitochondria and plastids. A comparison of evolutionary rates among these haploid genomes reveals striking parallels. Evidence suggests that haploid selection has the potential to shape evolution in predominantly diploid organisms, and taking advantage of the rapidly developing technologies, we are now in the position to quantify the importance of such selection on haploid genomes

Effects of ovarian fluid on sperm traits and its implications for cryptic female choice in zebrafish

In polyandrous mating systems, females maintain the opportunity to bias male fertilization success after mating in a process known as cryptic female choice. Mechanisms of cryptic female choice have been described both in internal and external fertilizers, and may affect fertilization processes at different stages before, during, and after fertilization. In internal fertilizers, females have substantial control over sperm storage and fertilization, whereas in external fertilizers, female control is limited. A key factor proposed to mediate cryptic female choice is the fluid surrounding the eggs, the ovarian fluid, as it may directly affect sperm performance. Here, we studied the role of ovarian fluid in post-mating sexual selection using the zebrafish, Danio rerio. Firstly, we assessed how ovarian fluid affects sperm swimming performance compared with freshwater. We focused on sperm motility, velocity, swimming trajectory, and longevity, all traits associated with competitive fertilization success in externally fertilizing fish. In a second step, we used a North Carolina II design to explore female, male, and female x male effects by testing sperm motility of 2 males in the ovarian fluid of 2 females in a total of 11 blocks. Our results indicate that the ovarian fluid affects sperm performance differently from freshwater. Specifically, sperm velocity, motility, and longevity were higher in the ovarian fluid than in freshwater, whereas sperm linearity and beat cross frequency showed the opposite pattern. Moreover, these effects varied according to male, female, and male x female identities, supporting the potential for cryptic female choice mediated by ovarian fluid in this species

The Evolutionary Consequences of Selection at the Haploid Gametic Stage

As an immediate consequence of sexual reproduction, biphasic life cycles with alternating diploid and haploid phases are a common characteristic of sexually reproducing eukaryotes. Much of our focus in evolutionary biology has been directed toward dynamics in diploid or haploid populations, but we rarely consider selection occurring during both phases when studying evolutionary processes. One of the reasons for this apparent omission is the fact that many flowering plants and metazoans are predominantly diploid with a very short haploid gametic phase. While this gametic phase may be short, it can play a crucial role in fundamental processes including the rate of adaptation, the load of mutation, and the evolution of features such as recombination. In addition, if selection acts in different directions between the two phases, a genetic conflict will occur, impacting the maintenance of genetic variation. Here we provide an overview of theoretical and empirical studies investigating the importance of selection at the haploid gametic phase in predominantly diploid organisms and discuss future directions to improve our understanding of the underlying dynamics and the general implications of haploid selection

Brains and the city: big-brained passerine birds succeed in urban environments

Urban regions are among the most humanaltered environments on Earth and they are poised for rapid expansion following population growth and migration. Identifying the biological traits that determine which species are likely to succeed in urbanized habitats is important for predicting global trends in biodiversity. We provide the first evidence for the intuitive yet untested hypothesis that relative brain size is a key factor predisposing animals to successful establishment in cities. We apply phylogenetic mixed modelling in a Bayesian framework to show that passerine species that succeed in colonizing at least one of 12 European cities are more likely to belong to big-brained lineages than species avoiding these urban areas. These data support findings linking relative brain size with the ability to persist in novel and changing environments in vertebrate populations, and have important implications for our understanding of recent trends in biodiversity.Peer Reviewe

Selection for longer-lived sperm within ejaculate reduces reproductive ageing in offspring

Males produce numerous sperm in a single ejaculate that greatly outnumber their potential egg targets. Recent studies found that phenotypic and genotypic variation among sperm in a single ejaculate of a male affects the fitness and performance of the resulting offspring. Specifically, within-ejaculate sperm selection for sperm longevity increased the performance of the resulting offspring in several key life-history traits in early-life. Because increased early-life reproductive performance often correlates with rapid ageing, it is possible that within-ejaculate sperm selection increases early-life fitness at the cost of accelerated senescence. Alternatively, within-ejaculate sperm selection could improve offspring quality throughout the life cycle, including reduced age-specific deterioration. We tested the two alternative hypotheses in an experimental setup using zebrafish Danio rerio. We found that within-ejaculate sperm selection for sperm longevity reduced age-specific deterioration of fecundity and offspring survival but had no effect on fertilization success in males. Remarkably, we found an opposing effect of within-ejaculate sperm selection on female fecundity, where selection for sperm longevity resulted in increased early-life performance followed by a slow decline, while females sired by unselected sperm started low but increased their fecundity with age. Intriguingly, within-ejaculate sperm selection also reduced the age-specific decline in fertilization success in females, suggesting that selection for sperm longevity improves at least some aspects of female reproductive ageing. These results demonstrate that within-ejaculate variation in sperm phenotype contributes to individual variation in animal life histories in the two sexes and may have important implications for assisted fertilization programs in livestock and humans

Accounting for the genetic load in assisted reproductive technology

The genetic load in the human genome has important ramifications for assisted reproductive technology (ART), human reproduction and fertility more generally. Here, we discuss these topics in the light of evolutionary genetic theory, the technological revolution in ART and the advances in the fields of genomics and bioinformatics

Individual variation in male mating preferences for female coloration in a polymorphic cichlid fish

Female color polymorphisms are common in the cichlid species radiations of Lake Victoria and Lake Malawi. According to theory, when a population harbors variation in sex-determining factors, polymorphism in female-linked coloration might generate individual variation in male mating preferences for female color morphs. We tested whether individual males exhibit consistent mating preferences for female color morphs in the Lake Malawi cichlid Pseudotropheus (Maylandia) ‘zebra gold', a species polymorphic for female coloration and sex determination. We also explored whether male mating preferences could be predicted by maternal coloration or were acquired by imprinting on siblings' coloration. We found large individual variation in the strength and direction of male preferences for sex-linked female color patterns. Male mating preferences could be predicted by the mother's color morph and were not affected by visual imprinting. These findings represent the first evidence of male choice on sex-linked female coloration in a Lake Malawi cichlid. Our analysis indicates a strong genetic component to male preference for female coloration and large individual variation in the strength and direction of male mating preferences. Within-population variation in innate mating preferences might have important implications in cichlid fish species radiation