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Selection for increased female reproductive investment generates males that harm their female partners

Selection can act in different ways in males and in females, and morphological, behavioural and physiological characteristics thus often show sex-specific optimal expression. Because a large part of the genome is shared between males and females of the same species, these sex-specific optima can result in a conflict between the sexes (INTRA-locus sexual conflict), with certain characteristics that are beneficial for one sex, are detrimental for the other. There are numerous examples of intralocus sexual conflict. For example, in humans, wide hips are beneficial for a smooth labour in women, whereas men benefit of having narrow hips for walking. Then, an evolutionary trade-off exists in the expression of genes modulating hip size. The result is that the net expression is neither optimal for males, nor females.

 In addition to such intra-locus conflicts, there are also INTER-locus sexual conflicts, where the male and female prospects about reproductive interactions differ. Frequently, males benefit of obtaining multiple copulations, whereas females tend to be harmed if they are involved in numerous copulations. This discrepancy leads to the evolution of selfish male strategies, such as coercive behaviours or toxic ejaculates. A classic example is seminal proteins of the fruit flies (Drosophila melanogaster). These substances generate benefits for males by increasing the females’ egg production, but, at the same time, are harmful for females by increasing their mortality risk. Females have been found to develop defense tools against such harmful male strategies, and males, in turn, new strategies for defeating the new female defence tools, and so on. This triggers an evolutionary tug-of-war between both sexes, with adaptations and counter-adaptations of males and females that accelerates evolutionary change. Male-induced harm in females has been well studied in invertebrates, but if similar processes take place in vertebrates is not clear. Furthermore, due to their different origins and consequences, the two forms of sexual conflict, intralocus and interlocus, have been considered independent forces. Yet, they have the potential to interact, thereby influencing the escalation or resolution of conflicts between the sexes.

 Researchers from the University of Exeter (United Kingdom) in collaboration with researchers from the Institute for Game and Wildlife Research (IREC, CSIC-UCLM-JCCM) have studied if males can harm females through the ejaculate in birds. With this purpose, selection lines of Japanese quail (Coturnix japonica) for a high or low reproductive investment have been established. (FIGURE 1)

 After several generations of selection, females of the high reproductive investment lines laid larger eggs, whereas females of the low reproductive investment lines laid smaller eggs. Although the selection was female-limited, it had correlated responses in males. Males from the high reproductive investment lines had a higher reproductive success than males from the low reproductive investment lines, potentially because they produce a better ejaculate. (FIGURE 2)

 In this study, the researchers discovered that males of the high reproductive investment lines generated more damage in the oviduct of their female partners when copulating (higher levels of a biological marker of stress and deterioration) than males of the low reproductive investment lines. This result was independent of the selection line of the female, so the line origin of the male exclusively caused this effect. Besides, the harm was restricted to the oviduct and not found in other tissues, suggesting that it was ejaculate-mediated. (FIGURE 3)

 This study is the first showing that the male ejaculate may harm the reproductive tract of the female in a vertebrate species (a bird). In addition, it shows that the male potential to generate harm is genetically linked to the female reproductive investment in the egg. Thus, this male ability to harm females may constraint the evolution of the female reproductive investment and be the origin, at least in part, of the natural differences in the reproductive investment between individuals and populations.

 However, the implications of this study go beyond. Here, there is an interlocus sexual conflict (males damaging females during copulation) whose origin is an intralocus sexual conflict (the investment in the egg of the female and the capacity to harm of the male are regulated by the same genes). This connection between intra- and interlocus sexual conflicts is very novel and challenges the evolutionary theory about sexual conflict. 

 

Pictures

  • Figure 1: Male (left) and female (right) Japanese quail (photos by Dennis Hansen).
  • Figure 2: Selection lines, figure from Pick et al 2016 (Heredity). Here, the selection process of...
  • Figure 3: Oviduct oxidative damage depending on male origin
  • female Japanese quail (Pic: Dennis Hansen)