Encyclopedia of Evolutionary Psychological Science

Living Edition
| Editors: Todd K. Shackelford, Viviana A. Weekes-Shackelford

Semen Toxicity

  • Mariana F. WolfnerEmail author
  • Tracey ChapmanEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-3-319-16999-6_3081-1

Keywords

Reproductive Success Seminal Fluid Sexual Conflict Female Longevity Female Lifespan 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Synonyms

Definition

In some taxa, molecules in the ejaculate can lower the longevity of females that receive them.

Introduction

Mating requires cooperation between the sexes. In species in which there are separate sexes, females and males of the same species must communicate to find each other, and sperm and eggs need to be united in the correct manner to achieve fertilization. And, at least in some organisms with parental care, cooperation between parents continues after the progeny are produced. Yet, against this background of cooperation, there are less salutary interactions. For example, in some taxa, males transfer in their seminal fluid molecules that result in premature death of their mates (e.g., in the fruit fly Drosophila melanogaster, nematode worm Caenorhabditis elegans, bean beetle Callosobruchus maculatus, Colorado potato beetle Leptinotarsa decemlineata (see Chapman et al. 1995; Shi and Murphy 2014 for examples)) or interfere with the function of other males’ sperm (a point that even merited mention in an episode of the TV series House). How and why would this occur?

Males and Females Have Different Reproductive Strategies

Males and females have a shared reproductive interest in passing on their genetic material to as many high-quality offspring as possible. But strategies to best achieve this may often differ between the sexes (e.g., see Chapman et al. 2003 for review). Egg production requires a large energetic investment that may outweigh investment in sperm or seminal fluids. In some organisms, progeny care and feeding are also disproportionately performed by females, requiring additional energy expenditure. Thus, it is often advantageous to females to mate selectively and use the sperm from the highest-quality males to fertilize their gametes. Phenomena such as limiting the extent of multiple mating, or increasing pair-bonding, may be useful strategies in this regard. Males, in contrast, may often benefit from adopting a very different strategy. With gametes that are energetically cheap to produce and can be made in very large numbers, males can benefit from mating multiply and frequently, with less regard to mate quality – it is a numbers game. When males are abundant, this can manifest as polyandry (more than one male mating with a given female), provided that this is not diluted by male social dominance strategies. When more than one male has mated with a female there is competition among the males’ sperm/ejaculates for fertilization opportunities. In a competitive situation such as this, any modification that can increase a male’s access to fertilization opportunities will increase his reproductive success and that of his male descendants who display it. Thus, over evolutionary time strategies such as increased sperm numbers and faster, “better,” sperm may be selected for.

Seminal Proteins Are Critical Contributors to Reproductive Success

A very important contributor to male reproductive success is the set of molecules that males make and transfer (along with sperm) to females during mating. These molecules include seminal proteins, whose effects can promote the success of their “own” sperm by harming the sperm of rival males. This was demonstrated in Hymenoptera (bees and ants; den Boer et al. 2010) in which sperm viability is decreased when sperm are incubated in seminal fluid of a different male (relative to within their own seminal fluid).

Seminal proteins also affect females in important, reproduction-enhancing ways, in all animals thus far examined (e.g., Avila et al. 2011 for insects). Within the female, seminal proteins access and act upon the neuroendocrine and reproductive systems, resulting in physiological changes that impact the female’s reproductive efficiency. For example, beta-NGF in the seminal fluid triggers female camelids to ovulate (Ratto et al. 2012), and an unrelated seminal protein, ovulin (Rubinstein and Wolfner 2013), does so in Drosophila melanogaster fruit flies. These actions ensure that eggs are quickly available to be fertilized by the male’s sperm, an outcome that is advantageous to the reproductive success of both the male and the female.

Differences in Reproductive Strategies Impact Seminal Protein Evolution

It is thought that seminal fluid proteins may have been selected initially in order to coordinate the many complex reproductive processes that need to be initiated following mating. Hence, seminal fluid proteins allow the matching of the timing of the cascade of reproductive changes in females that must occur in order to achieve successful fertilization. Such effects would be mutually beneficial for both sexes. For example, the female could “use” the male’s provision of seminal fluid to regulate her physiology to increase energy-demanding egg production only after mating has occurred and thus not “waste” energy on producing and ovulating eggs that cannot be fertilized and will die.

However, once there was the opportunity for males to influence the reproductive investment of females, particularly in polyandrous species, the stage was set for males to potentially “manipulate” female physiology and benefit male fertility or competitive success even if exacting costs in females. The different optimal reproductive strategies for males and females means that seminal proteins can be selected for that are advantageous to males, even if their effects might not benefit females. For example, seminal fluid of insect males contains molecules that decrease their mates’ propensity to remate (Avila et al. 2011). This effect can increase a male’s relative reproductive success by decreasing the likelihood that his sperm will be usurped by a rival’s or that his progeny will be in competition with half siblings from subsequent reproductive episodes by the same mother. Although this remating inhibition can potentially provide some benefit to the female (giving her more time to lay eggs and avoiding any negative physical consequences of mating itself), this effect of seminal proteins also decreases the female’s likelihood of mating with a “better” second male. In this sense, the interests of males and females are in conflict, with the seminal protein benefitting the male to the potential detriment of the female.

As long as a strategy benefits a male relative to his rivals, it can be selected for even if it causes harm to the female. If the negative effects of a seminal protein are large enough, female resistance can evolve, for example, by selection for mutations that make receptors for the seminal protein less abundant or less active or by increasing the amount or activity of seminal-protein degrading enzymes. This in turn can favor the emergence of new mechanisms in males to circumvent resistance, such as alternative strategies to prevent remating. An interesting example in this regard is the Drosophila “sex peptide” seminal protein. One function of this peptide is to decrease the female’s propensity to remate (Chen et al. 1988). Decreased remating propensity is most effective for the male if it persists as long as his sperm are available in the female to fertilize eggs. Interestingly, the sex peptide becomes attached to sperm, which maintains it in the female as long as sperm are present while protecting it from degradation by proteases in her circulatory system. Kubli and colleagues suggest that the development of sperm binding as a way to retain and protect sex peptide in the female may have led to the evolution of very long Drosophila sperm: males can retain more sex peptide in females this way. A number of studies have provided evidence for such an “arms race” of evolution of molecules and strategies by males, followed by counter-evolution of the females to resist harm, leading to new male strategies.

Semen Toxicity Occurs in Some Taxa and Likely Relates to the Sexes’ Differing Reproductive Strategies

A striking example of a situation in which males benefit at a clear cost to females is that seminal proteins decrease the longevity of females in some taxa (e.g., Chapman et al. 1995; Shi and Murphy 2014). Some decrease in female longevity as a cost of mating seems unsurprising. The energetic cost of producing eggs and progeny can trade off against somatic maintenance and health. However, if such earlier death is balanced by the benefits of having more progeny, especially early in life, then there is no overall net fitness cost. In order to attribute costs of mating to the receipt of seminal fluids, it is therefore important to consider the net outcomes of lifespan versus reproductive success. For example, when the source of the cost of mating (Fowler and Partridge 1989) was probed genetically in Drosophila melanogaster, it was found that there were additional costs besides increased egg production. In particular, a component of seminal fluid caused premature death of the female (Chapman et al. 1995). In experiments in which egg production and male exposure/harassment levels were controlled, females that mated repeatedly with males that supplied seminal proteins died sooner than females that had mated with males that did not supply seminal proteins. Thus, a seminal protein(s) decreased female longevity. Subsequent experiments showed that a particular seminal protein, the Drosophila-specific sex peptide, caused decreased female longevity (Wigby and Chapman 2005), although overexpression assays suggested that several other seminal proteins might also have a negative effect on female lifespan.

How and why can a seminal protein, like the sex peptide, result in significant harm to females? The reasons are as yet unknown but we can make some guesses. One possibility is that the sex peptide’s negative effects on female lifespan could be an “intended” and directly selected function that is actively selected for. Such an explanation would suggest that it is advantageous to the male to cause his mate to die soon after mating, either so that she would rapidly produce progeny as a terminal investment or so that her death would decrease the chances of her producing subsequent offspring with a rival. Although this is a formal possibility, there is as yet no experimental support for it.

An alternative hypothesis is that the female’s longevity decrease is not a direct consequence of the effect of sex peptide but is instead a side effect of some other, beneficial, effect. In this model, there would have been selection for the effects of sex peptide and the female response system to be tuned to balance the fertility-enhancing benefits of the male peptide with females being sufficiently resistant to its negative effects on longevity so as to have minimal impact on net fitness. Consistent with this interpretation, the effects of mating on female longevity in Drosophila are small – multiple matings are needed before a statistically significant longevity decrease is observed – and the increase in female death rate occurs after at least the initial burst of progeny production is completed. At the moment, we do not know which of the sex peptide’s many effects could result in this indirect but negative effect on female longevity, but there are several possibilities. First, the sex peptide increases feeding by females. Increased feeding is also required to provide increased nutrition to meet the energy expenditure of egg production. However, since increased caloric intake is also associated with decreased longevity in many organisms including Drosophila, feeding stimulation by sex peptide could have negative consequences on longevity. A second possibility is that sex peptide also decreases siesta sleep in mated females, improving their chance of finding egg-laying sites but also perhaps resulting in increased energy expenditure that could lead to earlier death. The sex peptide also induces immune gene expression in females, and it is possible, but is not yet demonstrated, that a high level of immune-gene expression could reduce female viability either due to increased energy expenditure on immune proteins or perhaps due to deleterious effects on the female’s microbiome. Finally, sex peptide changes hormone levels (juvenile hormone) in mated females; the shift in hormonal milieu could potentially be costly. In all cases, the positive effects of sex peptide on reproduction would have outweighed these negative side effects.

Although costs of semen receipt have been reported in a number of invertebrate taxa (e.g., Chapman et al. 1995; Shi and Murphy 2014) (it has not been searched for systematically in vertebrates), this phenomenon is not universal and is even context dependent in some taxa. Moreover, the one well-characterized inducer of early death in mated females – the sex peptide (Wigby and Chapman 2005) – is not found outside the genus Drosophila. And, not all Drosophila species show post-mating longevity decreases. For example, polyandry is reported as beneficial to female lifespan in D. simulans and in D. mojavensis increased mating confers resistance to desiccation stress. Hence different molecules and mechanisms may underlie costs observed in different taxa. This is consistent with our argument above that semen toxicity is not a directly selected effect. Rather, we suggest that in some taxa, a male-benefitting effect of a seminal protein may exact costs in females. Counterselection will keep the level of cost expressed in those taxa at a level that does not unduly impact upon net fitness, though some cost may be expressed as a pleiotropic effect of the beneficial reproductive effects of the seminal protein. Consistent with this, the toxicity of proteins that cause costs, and potentially even the type of toxicity they cause, are not expected to be conserved.

Conclusion

Semen toxicity represents a fascinating reflection of the fact that males and females use different strategies for optimal reproductive success. It will be intriguing to examine what has led to the evolution, and retention, of semen toxicity in some taxa but not in others.

Cross-References

References

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Copyright information

© Springer International Publishing AG 2016

Authors and Affiliations

  1. 1.Department of Molecular Biology and GeneticsCornell UniversityIthacaUSA
  2. 2.School of Biological SciencesUniversity of East AngliaNorwichUK

Section editors and affiliations

  • Catherine Salmon
    • 1
  1. 1.University of RedlandsRedlandsUSA