X-linked meiotic drive can boost population size and persistence

X-linked meiotic drivers cause X-bearing sperm to be produced in excess by male carriers, leading to female-biased sex ratios. Here, we find general conditions for the spread and fixation of X-linked alleles. Our conditions show that the spread of X-linked alleles depends on sex-specific selection and transmission rather than the time spent in each sex. Applying this logic to meiotic drive, we show that polymorphism is heavily dependent on sperm competition induced both by female and male mating behavior and the degree of compensation to gamete loss in the ejaculate size of drive males. We extend these evolutionary models to investigate the demographic consequences of biased sex ratios. Our results suggest driving X-alleles that invade and reach polymorphism (or fix and do not bias segregation excessively) will boost population size and persistence time by increasing population productivity, demonstrating the potential for selfish genetic elements to move sex ratios closer to the population-level optimum. However, when the spread of drive causes strong sex-ratio bias, it can lead to populations with so few males that females remain unmated, cannot produce offspring, and go extinct. This outcome is exacerbated when the male mating rate is low. We suggest that researchers should consider the potential for ecologically beneficial side effects of selfish genetic elements, especially in light of proposals to use meiotic drive for biological control.

Effects of condition and sperm competition risk on sperm allocation and storage in neriid flies

Ejaculate traits can be sexually selected and often exhibit heightened condition-dependence. However, the influence of sperm competition risk in tandem with condition-dependent ejaculate allocation strategies is relatively unstudied. Because ejaculates are costly to produce, high-condition males may be expected to invest more in ejaculates when sperm competition risk is greater. We examined the condition-dependence of ejaculate size by manipulating nutrient concentration in the juvenile (larval) diet of the neriid fly Telostylinus angusticollis. Using a fully factorial design we also examined the effects of perceived sperm competition risk (manipulated by allowing males to mate first or second) on the quantity of ejaculate transferred and stored in the three spermathecae of the female reproductive tract. To differentiate male ejaculates, we fed males nontoxic rhodamine fluorophores (which bind to proteins in the body) prior to mating, labeling their sperm red or green. We found that high-condition males initiated mating more quickly and, when mating second, transferred more ejaculate to both of the female’s posterior spermathecae. This suggests that males allocate ejaculates strategically, with high-condition males elevating their ejaculate investment only when facing sperm competition. More broadly, our findings suggest that ejaculate allocation strategies can incorporate variation in both condition and perceived risk of sperm competition.

Multiple biological mechanisms result in correlations between pre- and post-mating traits that differ among versus within individuals and genotypes

Reproductive traits involved in mate acquisition (pre-mating traits) are predicted to covary with those involved in fertilization success (post-mating traits). Variation in male quality may give rise to positive, and resource allocation trade-offs to negative, covariances between pre- and post-mating traits. Empirical studies have yielded mixed results. Progress is hampered as researchers often fail to appreciate that mentioned biological mechanisms can act simultaneously but at different hierarchical levels of biological variation: genetic correlations may, for example, be negative due to genetic trade-offs but environmental correlations may instead be positive due to individual variation in resource acquisition. We measured pre-mating (aggression, body weight) and post-mating (ejaculate size) reproductive traits in a pedigreed population of southern field crickets ( Gryllus bimaculatus ). To create environmental variation, crickets were raised on either a low or a high nymphal density treatment. We estimated genetic and environmental sources of correlations between pre- and post-mating traits. We found positive genetic correlations between pre- and post-mating traits, implying the existence of genetic variation in male quality. Over repeated trials of the same individual (testing order), positive changes in one trait were matched with negative changes in other traits, suggesting energy allocating trade-offs within individuals among days. These findings demonstrate the need for research on pre- and post-mating traits to consider the hierarchical structure of trait correlations. Only by doing so was our study able to conclude that multiple mechanisms jointly shape phenotypic associations between pre- and post-mating traits in crickets.

Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm

Gamete dimorphism (anisogamy) defines the sexes in most multicellular organisms. Theoretical explanations for its maintenance usually emphasize the size-related selection pressures of sperm competition and zygote survival, assuming that fertilization of all eggs precludes selection for phenotypes that enhance fertility. In external fertilizers, however, fertilization is often incomplete due to sperm limitation, and the risk of polyspermy weakens the advantage of high sperm numbers that is predicted to limit sperm size, allowing alternative selection pressures to target free-swimming sperm. We asked whether egg size and ejaculate size mediate selection on the free-swimming sperm of Galeolaria caespitosa , a marine tubeworm with external fertilization, by comparing relationships between sperm morphology and male fertility across manipulations of egg size and sperm density. Our results suggest that selection pressures exerted by these factors may aid the maintenance of anisogamy in external fertilizers by limiting the adaptive value of larger sperm in the absence of competition. In doing so, our study offers a more complete explanation for the stability of anisogamy across the range of sperm environments typical of this mating system and identifies new potential for the sexes to coevolve via mutual selection pressures exerted by gametes at fertilization.

Long-term effect of yolk carotenoid levels on testis size in a precocial bird

Conditions experienced during prenatal development can have long-lasting organizational effects on offspring. Maternal carotenoids deposited in the eggs of birds and other oviparous species play an important role during fast embryonic growth and chick development through their antioxidant properties. However, the long-term consequences of variation in maternal carotenoid transfer for the offspring have seldom been considered. Since plasma carotenoid levels at adulthood are known to influence testis size and yolk carotenoid levels influence the ability to extract carotenoids later in life, we hypothesized that maternally transmitted carotenoids might influence gonad size at adulthood. Here, we showed that male Japanese quail ( Coturnix japonica ) originating from a carotenoid-enriched egg had smaller testes than control individuals at adulthood. This result shows that yolk carotenoids have long-term organizational effects. In addition, given that carotenoid intake at sexual maturity increases sperm quality and that a decreased testis size is associated with a lower sperm production, we propose that carotenoid exposure during embryo development might influence a trade-off between ejaculate size and sperm quality.

Mating behavior and sexual selection in a polygamous beetle

Mating behavior and sexual selection in relation to morphometric traits in a polygamous beetle, Glenea cantor (F.) (Coleoptera: Cerambycidae), were investigated. Upon encounter, a male approached a female, mounted her, grasped her terminal abdomen with his hind tarsi, and attempted to mate. Successful mating lasted about 3.5 h. Although all traits measured in females and half of traits in males were significantly correlated with mating success, the primary selection on virgin females was the genital trait, the bursa copulatrix length, and that on males was the body length and hind tarsal length. Longer bursa copulatrix accommodated a larger ejaculate, suggesting that this female trait benefits the male that first mates with the female in terms of increasing ejaculate size to beat subsequent males in sperm competition. Under a female-biased sex ratio, more than 20% of matings failed within 20s after the male genitalia had been inserted into hers, suggesting that males assess genital features of the female before insemination and undertake cryptic male mate choice. Larger males were more capable of grasping females and achieving mating. During the premating struggle the male almost always used his hind tarsi to lift the female terminal abdomen to the position for his genitalia to insert, and as a result, males with longer hind tarsi achieved higher mating success.

Is sperm viability independent of ejaculate size in the house cricket (Acheta domesticus)?

Assessing sperm viability is a popular means of testing hypotheses related to ejaculate quality. This technique has produced interesting results; however, the sperm viability assay itself may kill sperm. This is a serious pitfall, as assay-related mortality could confound results and produce artificially low estimates of viability. To avoid spurious results, it has been recommended that investigators include sperm number in their viability analyses. Unfortunately, studies conducted to date on internal fertilizers have not included sperm counts in their analyses, so it is not possible to assess whether this factor can indeed produce artefactual results. In this paper, we use male house crickets ( Acheta domesticus (L., 1758)) to show that sperm viability is dependent on sperm number and exclusion of this factor from statistical analyses affects our interpretation of experimental treatment results. We show that mechanically rupturing a spermatophore significantly reduces sperm viability, but this does not appear to drive the nonindependent relationship between viability and number. Instead, our study shows that nonindependence is due to processes other than differential physical damage to the sperm during collection. We also show that allowing a spermatophore to evacuate its sperm without rupturing for 10 min maximizes both sperm number and viability.

Larger testes are associated with a higher level of polyandry, but a smaller ejaculate volume, across bushcricket species (Tettigoniidae)

While early models of ejaculate allocation predicted that both relative testes and ejaculate size should increase with sperm competition intensity across species, recent models predict that ejaculate size may actually decrease as testes size and sperm competition intensity increase, owing to the confounding effect of potential male mating rate. A recent study demonstrated that ejaculate volume decreased in relation to increased polyandry across bushcricket species, but testes mass was not measured. Here, we recorded testis mass for 21 bushcricket species, while ejaculate (ampulla) mass, nuptial gift mass, sperm number and polyandry data were largely obtained from the literature. Using phylogenetic-comparative analyses, we found that testis mass increased with the degree of polyandry, but decreased with increasing ejaculate mass. We found no significant relationship between testis mass and either sperm number or nuptial gift mass. While these results are consistent with recent models of ejaculate allocation, they could alternatively be driven by substances in the ejaculate that affect the degree of polyandry and/or by a trade-off between resources spent on testes mass versus non-sperm components of the ejaculate.