Sheri L. Johnson

Consistent age-dependent declines in human semen quality: A systematic review and meta-analysis

Reduced fertility typically occurs among women in their late 30s, but increasing evidence indicates that advanced paternal age is associated with changes in reproduction as well. Numerous studies have investigated age-based declines in semen traits, but the impact of paternal age on semen parameter values remains inconclusive. Using data from 90 studies (93,839 subjects), we conducted a systematic review and meta-analysis to quantify the effect of male age on seven ejaculate traits (semen volume, sperm concentration, total sperm count, morphology, total motility, progressive motility and DNA fragmentation). Age-associated declines in semen volume, percentage motility, progressive motility, normal morphology and unfragmented cells were statistically significant and results generally seemed to be robust against confounding factors. Unexpectedly, sperm concentration did not decline with increasing male age, even though we found that sperm concentration declined over time. Our findings indicate that male age needs more recognition as a potential contributor to the negative pregnancy outcomes and reduced offspring health associated with delayed first reproduction. We suggest that greater focus on collection of DNA fragmentation and progressive motility in a clinical setting may lead to better patient outcomes during fertility treatments of aging couples.

Remarkable Longevity of Dilute Sperm in a Free-Spawning Colonial Ascidian

Many benthic marine invertebrates reproduce by releasing sperm into the sea (free-spawning), but the amount of time that sperm are viable after spawning may have different consequences for fertilization, depending on the type of free-spawner. In egg-broadcasting marine organisms, gamete age is usually assumed to be irrelevant because of the low probability of contact between dilute sperm and egg. However, direct dilution effects might be reduced in egg-brooding free-spawners that filter dilute sperm out of the water column, and sperm longevity may play a role in facilitating fertilization in these taxa. We investigated the effects of time, temperature, and mixing on the viability of naturally released sperm of the colonial ascidian Botryllus schlosseri. Our data indicate that B. schlosseri sperm have a functional life span that is considerably longer than those of the sperm of many other marine invertebrate taxa (half-life of ∼16 to 26 h), are able to fertilize eggs at extremely low external sperm concentrations (ca. 101 sperm ml−1), and have a longevity that varies with temperature. It is possible that such prolonged sperm longevity may be achieved by reductions in motility, reactivation of quiescent sperm by chemical cues, or intermittent swimming.

Variation in multiple paternity in natural populations of a free‐spawning marine invertebrate

For free‐spawning marine invertebrates, fertilization processes control the genetic diversity of offspring. Each egg can potentially be fertilized by a sperm from a different male, and hence genetic diversity within a brood varies with levels of multiple paternity. Yet, few studies have characterized the frequency of multiple paternity in natural spawns. We analysed patterns of multiple paternity in two populations of the colonial ascidian Botryllus schlosseri using microsatellites. Because previous studies have shown that at moderate to high population densities, competition among male‐phase B. schlosseri colonies results in the nearest male dominating the paternity of a brood, we specifically tested the effect of population density on patterns of paternity. Paternity was estimated using three multilocus indices: minimum number of fathers, counts of sperm haplotypes, and effective paternity (KE). Multiple paternity was evident in more than 92% of the broods analysed, but highly variable, with a few broods displaying unequal contributions of different males. We found no effect of population density on multiple paternity, suggesting that other factors may control paternity levels. Indirect benefits from increasing the genetic diversity of broods are a possible explanation for the high level of multiple paternity in this species.

Are old males still good males and can females tell the difference

Sperm function generally declines with male age. Paradoxically, females of many species still choose to mate with old males rather than young males. Females choosing old mates may suffer reduced fertilization rates and an increased incidence of birth defects in offspring, lowering fitness which may in turn lead to conflict between the sexes. This apparent paradox has generated much interest from theorists, but whether this paradox presents in nature remains equivocal. Empirical studies have found mixed support for both a decline in fertility with male age and age‐based female mate preference. Here, we examine recent evidence for this paradox, identify confounding variables, highlight areas that deserve further investigation, and suggest avenues for future research.

Costs of multiple mates: an experimental study in horseshoe crabs

Why do females mate with multiple males? Since females often acquire all the sperm they need in one mating and since mating is usually costly, the evolution of polyandry is puzzling. Females may gain from mating multiply by ensuring fertilization, increasing offspring diversity, improving mate quality (‘good genes’) or increasing genetic compatibility. Alternatively, multiple mating may result in a net cost to females as a by-product of male–male competition. We report on field experiments in which we evaluated whether spawning with multiple males is costly or beneficial for female horseshoe crabs, Limulus polyphemus . Unpaired male horseshoe crabs crowd around some spawning pairs (polyandrous) as satellites while ignoring others (monandrous). We conducted three field experiments in which we compared the success of (1) unmanipulated polyandrous and monandrous females, (2) polyandrous females with and without satellites (satellites removed) and (3) monandrous females without and with satellites (forced to be polyandrous by adding satellites). When polyandrous females lost their satellite males, they laid more eggs than did polyandrous females that retained their satellites. When a satellite male arrives at a monandrous pair, some females are tolerant and will nest as a polyandrous female, but many females are intolerant of satellite males and leave immediately, thus laying fewer eggs. These results indicate that spawning with multiple males is costly in terms of nesting success for female horseshoe crabs. Yet, natural monandrous and polyandrous females did equally well, suggesting that there are compensating benefits from multiple males for polyandrous females. We suggest that monandry and polyandry may be alternative reproductive tactics for female horseshoe crabs.

Proteomic analysis of chinook salmon (Oncorhynchus tshawytscha) ovarian fluid.

The ovarian, or coelomic, fluid that is released with the egg mass of many fishes is increasingly found to play an important role in several biological processes crucial for reproductive success. These include maintenance of oocyte fertility and developmental competence, prolonging of sperm motility, and enhancing sperm swimming speed. Here we examined if and how the proteome of chinook salmon (Oncorhynchus tshawytscha) ovarian fluid varied among females and then sought to examine the composition of this fluid. Ovarian fluid in chinook salmon was analyzed using 1D SDS PAGE and LC-MS/MS tryptic digest screened against Mascot and Sequest databases. We found marked differences in the number and concentrations of proteins in salmon ovarian fluid across different females. A total of 174 proteins were identified in ovarian fluid, 47 of which were represented by six or more peptides, belonging to one of six Gene Ontology pathways. The response to chemical stimulus and response to hypoxia pathways were best represented, accounting for 26 of the 174 proteins. The current data set provides a resource that furthers our understanding of those factors that influence successful egg production and fertilisation in salmonids and other species.

The role of age on sperm traits in the American horseshoe crab, Limulus polyphemus

Sperm competition is an important component of postcopulatory sexual selection. Despite the fact that sperm traits may be important in determining fitness and thus may be under directional selection, they are often highly variable in mating systems with intense sperm competition. One possible explanation for this variation is that sperm traits vary with age. Age affects the expression of many life-history traits and sexual selection signals, but its influence on sperm traits is not well understood. In this study, we examined the correlation between individual age and sperm traits in a natural population of the American horseshoe crab. We compared five sperm traits (ejaculate size, concentration, total sperm ejaculated, velocity and viability) between males of three age categories. Young males ejaculated more total sperm and had significantly more concentrated sperm than old males. Males of different ages did not differ in sperm velocity or viability. Our results suggest that age influences traits associated with sperm quantity more than it does traits associated with sperm quality. Our results also suggest that individual age may be an important, but often overlooked, factor in studies examining sperm traits in natural populations.

The role of non-genetic inheritance in evolutionary rescue: epigenetic buffering, heritable bet hedging and epigenetic traps

Abstract Rapid environmental change is predicted to compromise population survival, and the resulting strong selective pressure can erode genetic variation, making evolutionary rescue unlikely. Non-genetic inheritance may provide a solution to this problem and help explain the current lack of fit between purely genetic evolutionary models and empirical data. We hypothesize that epigenetic modifications can facilitate evolutionary rescue through ‘epigenetic buffering’. By facilitating the inheritance of novel phenotypic variants that are generated by environmental change—a strategy we call ‘heritable bet hedging’—epigenetic modifications could maintain and increase the evolutionary potential of a population. This process may facilitate genetic adaptation by preserving existing genetic variation, releasing cryptic genetic variation and/or facilitating mutations in functional loci. Although we show that examples of non-genetic inheritance are often maladaptive in the short term, accounting for phenotypic variance and non-adaptive plasticity may reveal important evolutionary implications over longer time scales. We also discuss the possibility that maladaptive epigenetic responses may be due to ‘epigenetic traps’, whereby evolutionarily novel factors (e.g. endocrine disruptors) hack into the existing epigenetic machinery. We stress that more ecologically relevant work on transgenerational epigenetic inheritance is required. Researchers conducting studies on transgenerational environmental effects should report measures of phenotypic variance, so that the possibility of both bet hedging and heritable bet hedging can be assessed. Future empirical and theoretical work is required to assess the relative importance of genetic and epigenetic variation, and their interaction, for evolutionary rescue.

Evidence of a Native Northwest Atlantic COI Haplotype Clade in the Cryptogenic Colonial Ascidian Botryllus schlosseri.

The colonial ascidian Botryllus schlosseri should be considered cryptogenic (i.e., not definitively classified as either native or introduced) in the Northwest Atlantic. Although all the evidence is quite circumstantial, over the last 15 years most research groups have accepted the scenario of human-mediated dispersal and classified B. schlosseri as introduced; others have continued to consider it native or cryptogenic. We address the invasion status of this species by adding 174 sequences to the growing worldwide database for the mitochondrial gene cytochrome c oxidase subunit I (COI) and analyzing 1077 sequences to compare genetic diversity of one clade of haplotypes in the Northwest Atlantic with two hypothesized source regions (the Northeast Atlantic and Mediterranean). Our results lead us to reject the prevailing view of the directionality of transport across the Atlantic. We argue that the genetic diversity patterns at COI are far more consistent with the existence of at least one haplotype clade in the Northwest Atlantic (and possibly a second) that substantially pre-dates human colonization from Europe, with this native North American clade subsequently introduced to three sites in Northeast Atlantic and Mediterranean waters. However, we agree with past researchers that some sites in the Northwest Atlantic have more recently been invaded by alien haplotypes, so that some populations are currently composed of a mixture of native and invader haplotypes.

Population differentiation and behavioural association of the two ‘personality’ genes DRD4 and SERT in dunnocks (Prunella modularis)

Quantifying the variation in behaviour‐related genes within and between populations provides insight into how evolutionary processes shape consistent behavioural traits (i.e. personality). Deliberate introductions of non‐native species offer opportunities to investigate how such genes differ between native and introduced populations and how polymorphisms in the genes are related to variation in behaviour. Here, we compared the genetic variation of the two ‘personality’ genes, DRD4 and SERT, between a native (United Kingdom, UK) and an introduced (New Zealand, NZ) population of dunnocks, Prunella modularis. The NZ population showed a significantly lower number of single nucleotide polymorphisms (SNPs) compared to the UK population. Standardized F’st estimates of the personality genes and neutral microsatellites indicate that selection (anthropogenic and natural) probably occurred during and post the introduction event. Notably, the largest genetic differentiation was found in the intronic regions of the genes. In the NZ population, we also examined the association between polymorphisms in DRD4 and SERT and two highly repeatable behavioural traits: flight‐initiation distance and mating status (promiscuous females and cobreeding males). We found 38 significant associations (for different allele effect models) between the two behavioural traits and the studied genes. Further, 22 of the tested associations showed antagonistic allele effects for males and females. Our findings illustrate how introduction events and accompanying ecological changes could influence the genetic diversity of behaviour‐related genes.