Cryptic female choice within individual males - A neglected component of the postmating sexual selection?

Cryptic female choice (CFC) is commonly assumed to act only in polyandrous mating systems, which allows females to bias fertilization towards the sperm of particular males. However, accumulated evidence has demonstrated that sperm show significant phenotypic and genotypic variation also within single ejaculates, which have important consequences for offspring phenotype and fitness. Here, I argue that these neglected sources of intra-male sperm variation often allow CFC to act also within individual males and facilitate fertilization bias towards genetically compatible (or otherwise preferred) sperm haplotypes. In this article, I explain prerequisites for within-male CFC, the criteria for demonstrating it and summarize accumulated evidence for this emerging selection process. Then, I evaluate prevalence of within-male CFC and review its potential evolutionary consequences. The aim of this article is to broaden the current definition of CFC by demonstrating that CFC has potential to act in all mating systems, in both internally and externally fertilizing species. Incorporation of the within-male CFC concept into the current models of sexual selection may provide novel insights into the deeper understanding of selective factors driving the evolution of mating systems and reproductive proteins. Finally, within-male CFC towards particular sperm haplotypes may increase our understanding of non-Mendelian inheritance.

Female-induced selective modification of sperm protein SUMOylation-potential mechanistic insights into the non-random fertilization in humans.

In many species, mate choice continues after the mating via female- or egg-derived biochemical factors that induce selective changes in sperm pre-fertilization physiology and behaviour. Recent studies have indicated that gamete-mediated mate choice likely occurs also in humans, but the mechanistic basis of the process has remained virtually unexplored. Here, we investigated whether female-induced modifications in sperm protein SUMOylation (post-translational modification of the proteome) could serve as a novel mechanism for gamete-mediated mate choice in humans. We treated the sperm of ten males with the oocyte-surrounding bioactive liquid (follicular fluid) of five females and investigated motility, viability and global protein SUMOylation status of the sperm in all (n = 50) of these male-female combinations (full-factorial design). All the measured sperm traits were affected by male-female combinations, and sperm protein SUMOylation status was also negatively associated with sperm motility. Furthermore, our results indicate that female-induced sperm protein SUMOylation is selective, potentially allowing females to increase sperm motility in some males, whereas decreasing it in the others. Consequently, our findings suggest that follicular fluid may non-randomly modify the structure and function of sperm proteome and in this way facilitate gamete-mediated mate choice in humans and possibly many other species. However, due to the relatively low number of female subjects and their potential infertility problems, our results should be replicated with larger subset of fully fertile women.

Submicron Plastic Adsorption by Peat, Accumulation in Sphagnum Mosses and Influence on Bacterial Communities in Peatland Ecosystems.

The smallest fraction of plastic pollution, submicron plastics (SMPs <1 µm) are expected to be ubiquitous in the environment. No information is available about SMPs in peatlands, which have a key role in sequestering carbon in terrestrial ecosystems. It is unknown how these plastic particles might behave and interact with (micro)organisms in these ecosystems. Here, we show that the chemical composition of polystyrene (PS) and poly(vinyl chloride) (PVC)-SMPs influenced their adsorption to peat. Consequently, this influenced the accumualtion of SMPs by Sphagnum moss and the composition and diversity of the microbial communities in peatland. Natural organic matter (NOM), which adsorbs from the surrounding water to the surface of SMPs, decreased the adsorption of the particles to peat and their accumulation by Sphagnum moss. However, the presence of NOM on SMPs significantly altered the bacterial community structure compared to SMPs without NOM. Our findings show that peatland ecosystems can potentially adsorb plastic particles. This can not only impact mosses themselves but also change the local microbial communities.

Sperm Physiological Response to Female Serum-Potential New Insights into the Reproductive Incompatibility Diagnostics.

Infertility is assumed to arise exclusively from male- and female-dependent pathological factors. However, recent studies have indicated that reproductive failure may also result from the reproductive incompatibility of the partners. Selection against such incompatibilities likely occurs via female-derived reproductive secretions, including follicular fluid (FF), that mediate gamete-level mate choice towards the sperm of specific males. To facilitate potential development of diagnostic tests for human reproductive incompatibility, we examined whether sperm physiological response to female serum indicate male-female compatibility in the presence of FF. We performed a full-factorial experiment, in which the sperm of 10 males were treated with the FF and serum of 6 healthy females. We found that sperm motility and viability in both biofluids were highly similar and that in 70% of the males, sperm serum treatment predicted male-female compatibility. We also identified male human leucocyte antigen (HLA) alleles and female (FF and serum) anti-HLA antibodies and tested whether the number of allele-antibody matches predict sperm physiological response to female fluids. However, no association was found between measured sperm traits and the number of allele-antibody matches. Overall, the present results may open novel possibilities for the future development of reproductive incompatibility tests and may pave the way towards more accurate infertility diagnostics and treatments.

Genetic incompatibility of the reproductive partners: an evolutionary perspective on infertility.

In natural fertilisation, the female reproductive tract allows only a strictly selected sperm subpopulation to proceed in the vicinity of an unfertilised oocyte. Female-mediated sperm selection (also known as cryptic female choice (CFC)) is far from a random process, which frequently biases paternity towards particular males over others. Earlier studies have shown that CFC is a ubiquitous phenomenon in the animal kingdom and often promotes assortative fertilisation between genetically compatible mates. Here, I demonstrate that CFC for genetic compatibility likely also occurs in humans and is mediated by a complex network of interacting male and female genes. I also show that the relative contribution of genetic compatibility (i.e. the male-female interaction effect) to reproductive success is generally high and frequently outweighs the effects of individual males and females. Together, these facts indicate that, along with male- and female-dependent pathological factors, reproductive failure can also result from gamete-level incompatibility of the reproductive partners. Therefore, I argue that a deeper understanding of these evolutionary mechanisms of sperm selection can pave the way towards a more inclusive view of infertility and open novel possibilities for the development of more personalised infertility diagnostics and treatments.

Structural dissimilarity of partners' immune genes increases sperm viability in women's reproductive tract.

Human leucocyte antigen (HLA) genes appear to mediate pre- and post-copulatory mate choice towards HLA-dissimilar ('compatible') partners. However, since genetically distinct alleles often have similar immunogenic properties, genetic dissimilarity is not necessarily an accurate predictor of the functional compatibility of HLA alleles and, hence, may not reflect partners' true compatibility. Furthermore, it has remained unclear whether other genes of the immune system could also play a role in male-female compatibility. We studied whether the immunoglobulin binding regions (eplets) of HLA molecules and the immunoglobulin structural dissimilarity of the partners affect their gamete-level compatibility. We exposed sperm of multiple men to follicular fluid or cervical mucus of multiple women and tested whether sperm viability in these reproductive secretions was influenced by HLA eplet and immunoglobulin structural dissimilarity between partners. We found that eplet dissimilarity positively affects sperm viability in follicular fluid, whereas immunoglobulin dissimilarity enhanced sperm viability in cervical mucus. Together, these findings indicate that structural characteristics of both HLA alleles and immunoglobulins may facilitate cryptic female choice towards immunologically compatible partners. Our results, thus, indicate that partners' genetic compatibility may have wider immunological basis than traditionally has been assumed. Relative contribution of different immunogenetic factors to overall compatibility of the reproductive partners needs to be clarified in future studies.

Ultra-acute exposure to cadmium does not impair whitefish sperm motility.

Cadmium (Cd) exposure can impair the traits of aquatic animals associated with reproduction. In natural lakes Cd is typically detected at concentrations below 0.001 mg l-1 . The authors investigated the impact of ultra-acute Cd exposure on sperm motility in European whitefish (Coregonus lavaretus). They activated sperm with water containing various nominal concentrations of Cd and recorded sperm motility parameters. Only the highest Cd concentration (500 mg l-1 ) was associated with decreased sperm swimming velocity and increases in both the percentage of static cells and curvature of the sperm swimming trajectory. The results indicate that environmentally realistic concentrations of Cd during the sperm motility activation are not critically harmful to male C. lavaretus fertilization potential.

Post-copulatory genetic matchmaking: HLA-dependent effects of cervical mucus on human sperm function.

Several studies have demonstrated that women show pre-copulatory mating preferences for human leucocyte antigen (HLA)-dissimilar men. A fascinating, yet unexplored, possibility is that the ultimate mating bias towards HLA-dissimilar partners could occur after copulation, at the gamete level. Here, we explored this possibility by investigating whether the selection towards HLA-dissimilar partners occurs in the cervical mucus. After combining sperm and cervical mucus from multiple males and females (full factorial design), we found that sperm performance (swimming velocity, hyperactivation, and viability) was strongly influenced by the male-female combination. This indicates that sperm fertilization capability may be dependent on the compatibility between cervical mucus (female) and sperm (male). We also found that sperm viability was associated with partners' HLA dissimilarity, indicating that cervical mucus may selectively facilitate later gamete fusion between immunogenetically compatible partners. Together, these results provide novel insights into the female-mediated sperm selection (cryptic female choice) in humans and indicate that processes occurring after copulation may contribute to the mating bias towards HLA-dissimilar partners. Finally, by showing that sperm performance in cervical mucus is influenced by partners' genetic compatibility, the present findings may promote a deeper understanding of infertility.

Offspring phenotype is shaped by the nonsperm fraction of semen.

In a large majority of animal species, the only contribution of males to the next generation has been assumed to be their genes (sperm). However, along with sperm, seminal plasma contains a wide array of extracellular factors that have many important functions in reproduction. Yet, the potential intergenerational effects of these factors are virtually unknown. We investigated these effects in European whitefish (Coregonus lavaretus) by experimentally manipulating the presence and identity of seminal plasma and by fertilizing the eggs of multiple females with the manipulated and unmanipulated semen of several males in a full-factorial breeding design. The presence of both own seminal plasma and foreign seminal plasma inhibited sperm motility, and the removal of own seminal plasma decreased embryo survival. Embryos hatched significantly earlier after both semen manipulations than in control fertilizations; foreign seminal plasma also increased offspring aerobic swimming performance. Given that our experimental design allowed us to control potentially confounding sperm-mediated (sire) effects and maternal effects, our results indicate that seminal plasma may have direct intergenerational consequences for offspring phenotype and performance. This novel source of offspring phenotypic variance may provide new insights into the evolution of polyandry and mechanisms that maintain heritable variation in fitness and associated female mating preferences.

Gamete-level immunogenetic incompatibility in humans-towards deeper understanding of fertilization and infertility?

Human leukocyte antigen (HLA) immune genes play an important role in partner selection, but it has remained unclear if nonrandom pairing with respect to parental HLA genes could occur at the level of the gametes. We tested this possibility by investigating whether the sperm fertilization competence in humans is dependent on HLA genotype combination of the partners. We conducted a full-factorial experiment, in which the sperm physiological preparation for fertilization among multiple males was studied in the presence of follicular fluid (oocyte surrounding bioactive liquid) of several females. All the studied sperm pre-fertilization physiological parameters (motility, hyperactivation, acrosome reaction, and viability) were strongly dependent on male-female combination. In other words, follicular fluids (women) that induce strong sperm physiological response in some males often induce much weaker response in the other(s). Sperm physiological responses were stronger in HLA-dissimilar male-female pairs than in HLA-similar combinations, but none of the measured sperm traits were associated with genome-wide similarity. Together, these findings shed new light on the evolutionary and immunological mechanisms of fertilization. Furthermore, our results raise an intriguing possibility that against currently prevailing WHO's definition, infertility may not represent exclusively a pathological condition, but may also result from immunogenetic incompatibility of the gametes.

Gamete-mediated mate choice: towards a more inclusive view of sexual selection.

'Sperm competition'-where ejaculates from two or more males compete for fertilization-and 'cryptic female choice'-where females bias this contest to suit their reproductive interests-are now part of the everyday lexicon of sexual selection. Yet the physiological processes that underlie these post-ejaculatory episodes of sexual selection remain largely enigmatic. In this review, we focus on a range of post-ejaculatory cellular- and molecular-level processes, known to be fundamental for fertilization across most (if not all) sexually reproducing species, and point to their putative role in facilitating sexual selection at the level of the cells and gametes, called 'gamete-mediated mate choice' (GMMC). In this way, we collate accumulated evidence for GMMC across different mating systems, and emphasize the evolutionary significance of such non-random interactions among gametes. Our overall aim in this review is to build a more inclusive view of sexual selection by showing that mate choice often acts in more nuanced ways than has traditionally been assumed. We also aim to bridge the conceptual divide between proximal mechanisms of reproduction, and adaptive explanations for patterns of non-random sperm-egg interactions that are emerging across an increasingly diverse array of taxa.

Sperm pre-fertilization thermal environment shapes offspring phenotype and performance.

The sperm pre-fertilization environment has recently been suggested to mediate remarkable transgenerational consequences for offspring phenotype (transgenerational plasticity, TGB), but the adaptive significance of the process has remained unclear. Here, we studied the transgenerational effects of sperm pre-fertilization thermal environment in a cold-adapted salmonid, the European whitefish (Coregonus lavaretus). We used a full-factorial breeding design where the eggs of five females were fertilized with the milt of 10 males that had been pre-incubated at two different temperatures (3.5°C and 6.5°C) for 15 h prior to fertilization. Thermal manipulation did not affect sperm motility, cell size, fertilization success or embryo mortality. However, offspring that were fertilized with 6.5°C-exposed milt were smaller and had poorer swimming performance than their full-siblings that had been fertilized with the 3.5°C-exposed milt. Furthermore, the effect of milt treatment on embryo mortality varied among different females (treatment×female interaction) and male-female combinations (treatment×female×male interaction). Together, these results indicate that sperm pre-fertilization thermal environment shapes offspring phenotype and post-hatching performance and modifies both the magnitude of female (dam) effects and the compatibility of the gametes. Generally, our results suggest that short-term changes in sperm thermal conditions may have negative impact for offspring fitness. Thus, sperm thermal environment may have an important role in determining the adaptation potential of organisms to climate change. Detailed mechanism(s) behind our findings require further attention.

Metabolic rate associates with, but does not generate covariation between, behaviours in western stutter-trilling crickets, Gryllus integer.

The causes and consequences of among-individual variation and covariation in behaviours are of substantial interest to behavioural ecology, but the proximate mechanisms underpinning this (co)variation are still unclear. Previous research suggests metabolic rate as a potential proximate mechanism to explain behavioural covariation. We measured the resting metabolic rate (RMR), boldness and exploration in western stutter-trilling crickets, Gryllus integer, selected differentially for short and fast development over two generations. After applying mixed-effects models to reveal the sign of the covariation, we applied structural equation models to an individual-level covariance matrix to examine whether the RMR generates covariation between the measured behaviours. All traits showed among-individual variation and covariation: RMR and boldness were positively correlated, RMR and exploration were negatively correlated, and boldness and exploration were negatively correlated. However, the RMR was not a causal factor generating covariation between boldness and exploration. Instead, the covariation between all three traits was explained by another, unmeasured mechanism. The selection lines differed from each other in all measured traits and significantly affected the covariance matrix structure between the traits, suggesting that there is a genetic component in the trait integration. Our results emphasize that interpretations made solely from the correlation matrix might be misleading.

Infection ecology of Philometra ovata (Nematoda: Philometridae) in a wild European minnow (Phoxinus phoxinus) population in Finland.

Seasonal life cycle of body cavity dwelling (BCD) Philometra ovata (Nematoda: Philometridae) has been reported in southern and central European countries, but its swim bladder dwelling (SBD) stage and northern populations have remained unstudied. In this study, we investigated the seasonal life cycle and infection ecology of P. ovata in both swim bladder and body cavity in the European minnow (Phoxinus phoxinus) in Finland. The larval P. ovata infected the swim bladder of minnows mainly in August. Female SBD P. ovata emigrated to body cavity mostly in September, grew to their full size by the end of the next June, and evacuated from minnows in July. In addition, female SBD P. ovata retarding their development and staying in swim bladder were found commonly in minnows, thus the mean monthly prevalence (6·7 ± 3·9%) and mean intensity (1·4 ± 0·8) of BCD P. ovata was lower than that of SBD P. ovata (37·8 ± 15·1% and 2·0 ± 1·5, respectively). Finally, despite the large size of BCD individuals, infection of P. ovata did not impair body condition and relative gonad size of minnows, but increased the mortality and caused physical damages in their hosts during the evacuation period.

Comparative analysis of microbiome inhabiting oxygenated and deoxygenated habitats using V3 and V6 metabarcoding of 16S rRNA gene.

We examine how oxygen levels and the choice of 16S ribosomal RNA (rRNA) tags impact marine bacterial communities using Next-Generation amplicon sequencing. Analyzing V3 and V6 regions, we assess microbial composition in both Oxygen minimum zones (OMZ) and non-OMZ (NOMZ) areas in the Arabian Sea (AS) and the Central Indian Ocean basin (CIOB) respectively. Operational taxonomic units (OTUs) at 97% similarity showed slightly higher richness and diversity with V6 compared to V3. Vertical diversity patterns were consistent across both regions. NOMZ showed greater richness and diversity than OMZ. AS and CIOB exhibited significant differences in bacterial community, diversity, and relative abundance at the order and family levels. Alteromonadaceae dominated the OMZ, while Pelagibacteraceae dominated the NOMZ. Synechococcaceae were found exclusively at 250 m in OMZ. Bacteria putatively involved in nitrification, denitrification, and sulfurylation were detected at both sites. Dissolved oxygen significantly influenced microbial diversity at both sites, while seasonal environmental parameters affected diversity consistently, with no observed temporal variation.

Selection among critically endangered landlocked salmon (Salmo salar m. sebago) families in survival and growth traits across early life stages and in different environments.

Endangered wild fish populations are commonly supported by hatchery propagation. However, hatchery-reared fish experience very different selective pressures compared to their wild counterparts, potentially causing genotype-by-environment interactions (G × E) in essential fitness traits. We experimentally studied early selection in a critically endangered landlocked Atlantic salmon population, first from fertilization to the swim-up stage in a common hatchery setting, and thereafter until the age of 5 months in two contrasting rearing environments. Swim-up progeny were moved either to standard indoor hatchery tanks involving conventional husbandry or to seminatural outdoor channels providing only natural food. After the first summer, sampled survivors were assigned to their families by genotyping. Early survival until the swim-up stage was mostly determined by maternal effects, but also involved significant variation due to sires and full-sib families (potential genetic effects). High on-growing survival in hatchery tanks (88.7%) maintained a more even distribution among families (relative share 1.5%-4.2%) than the seminatural environment (0.0%-5.4%). This heterogeneity was mostly maternal, whereas no independent paternal effect occurred. Heritability estimates were high for body size traits in both environments (0.62-0.69). Genetic correlations between the environments were significantly positive for body size traits (0.67-0.69), and high body condition in hatchery was also genetically linked to rapid growth in the seminatural environment (0.54). Additive and phenotypic growth variation increased in the seminatural environment, but scaling effects probably played a less significant role for G × E, compared to re-ranking of genotypes. Our results suggest that not only maternal effects, but also genetic effects, direct selection according to the environmental conditions experienced. Consistently high genetic variation in growth implies that, despite its low overall genetic diversity and long history in captive rearing (>50 years), this landlocked Atlantic salmon population still possesses adaptive potential for response to change from hatchery rearing back to more natural conditions.

Female ornaments revisited - are they correlated with offspring quality?

The evolution and signalling content of female ornamentation has remained an enduring challenge to evolutionary biologists, despite the fact that secondary sexual characters are widespread in females. While females usually invest significant amounts of their resources, including carotenoids, in offspring, all the resources allocated to elaborate ornamentation reduce resources available for other purposes. This may in turn constrain female fitness leading to dishonest female signalling. We review the literature for empirical studies on mutually ornamented species with conventional sex roles, by focusing on the association between female ornaments and quality of their offspring. We found 43 papers where 33 (77%) are bird-studies, nine (21%) are on fishes, and one (2%) is a lizard-study. Nine of these report negative, 14 non-existing, and 20 positive associations between female ornament and offspring quality. Eighteen of the bird studies (55%) show a positive association between the two traits investigated, whereas five (15%) of the studies report a negative association. The number of fish studies, although few, is skewed in the opposite direction with two (22%) and four (44%) studies supporting positive and negative association, respectively. A minority of studies on carotenoids-based ornaments reports a positive association (4 of 18 studies, or 22%) between the traits, which is low compared to studies on non-carotenoids-based ornaments (16 of 25 studies, or 64%). The above-mentioned relative large number of studies with negative association, especially common in studies on fishes and in carotenoids-based-ornaments, challenges the generality of the direct selection hypothesis to account for female fineries. This is important because this hypothesis seems to have strong support in recent literature on the topic. In the present paper, we also propose possible explanations for the observed differences between taxa and suggest directions and ideas for future research on the evolution of female ornamentation.

Diversity and Quantitative Detection of Clade I Type nosZ Denitrifiers in the Arabian Sea Oxygen Minimum Zone.

A significant amount of nitrous oxide (N2O) is effluxed into the atmosphere as a result of marine denitrification in the Arabian Sea (AS) oxygen minimum zone (OMZ). An assessment of temporal variations in the diversity and abundance of nosZ denitrifiers was performed to establish the relative importance of these bacteria in denitrification. Sampling was conducted at the Arabian Sea Time Series (ASTS) location and a quantitative PCR (qPCR) ana-lysis was performed. We detected a high abundance of the nosZ gene at core OMZ depths (250| |m and 500 m), indicating the occurrence of denitrification in the AS-OMZ. The maximum abundance of the nosZ gene was observed during the Spring Intermonsoon (SIM) at 250| |m (1.32×106 copies L-1) and 500| |m (1.50×106 copies L-1). Sequencing ana-lysis showed that nosZ denitrifiers belonged to the classes Alpha-, Beta-, and Gammaproteobacteria. Taxonomic ana-lysis revealed that most OTUs were affiliated with Pseudomonas, Rhodopseudomonas, and Bradyrhizobium. Diversity indices and richness estimators confirmed a higher diversity of nosZ denitrifiers at 250| |m than at 500| |m during all three seasons. The present results also indicated that dissolved oxygen (DO) and total organic carbon (TOC) are critical factors influencing the diversity and abundance of the nosZ-denitrifying bacterial community.

Non-invasive diagnosis for Philometra ovata (Nematoda) infection in the common minnow Phoxinus phoxinus.

Non-invasive diagnoses for most of the extraintestinal helminth infections among vertebrates are rare. In the present study, we developed and tested a non-invasive visual diagnosis method to detect the infection of the nematode Philometra ovata, which is parasitising in the body cavity of the common minnow Phoxinus phoxinus. By observing the surface of minnow's abdomen, we diagnosed infected minnows with irregular or vermiform-shaped uplifts as a consequence of the presence of P. ovata in the body cavity. We conducted the diagnosis in minnows with or without anaesthetisation, and our results showed the non-invasive method is highly reliable (correct rate of diagnoses > 95 %) in both anaesthetised and non-anaesthetised groups. The correct rate of diagnoses in truly uninfected fish (i.e. specificity) was nearly 100 % in both groups, while the correct rate of diagnoses in truly infected fish (i.e. sensitivity) was 71 and 65 % in anaesthetised and non-anaesthetised fish, respectively. The correct rate in fish diagnosed as infected or uninfected (i.e. positive or negative predictive power) of non-invasive diagnosis was nearly 100 % among the anaesthetised fish, and over 95 % in non-anaesthetised group. The diagnosis also yielded prevalence of P. ovata infection similar to the real prevalence in anaesthetised fish. Diagnoses conducted by an inexperienced observer indicated that the method is repeatable. Taken together, the present non-invasive method seems to be a promising new tool for non-invasive detection of P. ovata infections in minnows and probably can be applied for the detection of other body cavity dwelling metazoan parasites in various host taxa.

Seminal-Plasma-Mediated Effects on Sperm Performance in Humans.

Seminal plasma (SP) plays a crucial role in reproduction and contains a large number of proteins, many of which may potentially modify sperm functionality. To evaluate the effects of SP identity and its protein composition on human sperm function, we treated the sperm of several males with either their own or multiple foreign SPs in all possible sperm-SP combinations (full-factorial design). Then we recorded sperm motility and viability in these combinations and investigated whether the sperm performance is dependent on sperm and SP identity (or their interaction). Finally, we studied whether the above-mentioned sperm traits are affected by the abundance of three SP proteins, dipeptidyl peptidase-4 (DPP4), neutral endopeptidase (NEP), and aminopeptidase N (APN). The identity of the SP donor affected sperm swimming velocity, viability, and the proportion of hyperactivated sperm, but males' own SP was not consistently more beneficial for sperm than foreign SPs. Furthermore, we show that sperm performance is also partly affected by the interaction between sperm and SP donor. Finally, we found that DPP4 and NEP levels in SP were positively associated with sperm swimming velocity and hyperactivation. Taken together, our results highlight the importance of seminal plasma as a potential source of biomarkers for diagnostics and therapeutic interventions for male-derived infertility.