Objective and subjective components of resource value in lethal fights between male entomopathogenic nematodes

Males sometimes engage in fights over contested resources such as access to mates; in this case, fighting behaviour may be adjusted based on the value they place on the females. Resource value (RV) can have two components. First, males can assess the quality of females, which constitutes an objective assessment of RV. Second, internal state such as previous mating experience can also influence motivation to fight thus constituting a subjective assessment of RV. If mating opportunities are scarce and available females have a major impact on the lifetime reproductive success of males, then fighting can be fatal; in this situation it is uncertain whether males would adjust fighting behaviour based on RV. We found that both female quality, that is, virginity (objective component of RV) and male mating status (subjective component of RV) influenced fighting intensity between males of the entomopathogenic nematode Steinernema longicaudum which engage in lethal fights. Male nematodes were more likely to engage in fighting and fought longer and more frequently in the presence of virgin (high-quality) females than in the presence of mated (lower-quality) females. Male mating status was also found to influence fighting behaviour: mated males were the winners in staged fights between mated and virgin males. Mated males may have superior fighting ability (greater resource-holding potential), but RV asymmetries between mated and virgin males cannot be excluded. Males were more likely to win when they were resident, but we did not find a significant interaction effect between male mating and residency status

Lethal Fighting in Nematodes Is Dependent on Developmental Pathway: Male-Male Fighting in the Entomopathogenic Nematode <i>Steinernema longicaudum</i>

<div><p>Aggressive encounters occur between competitors (particularly males) throughout the animal kingdom, and in some species can result in severe injury and death. Here we describe for the first time lethal interactions between male nematodes and provide evidence that the expression of this behaviour is developmentally controlled. Males of the entomopathogenic nematode <i>Steinernema longicaudum</i> coil around each other, resulting in injuries, paralysis and frequently death. The probability of death occurring between pairs of males was affected by the developmental pathway followed, being much greater among males that had passed through the infective juvenile (IJ, or dauer) stage than among males that had not. Post-IJ males are found only in newly colonised hosts, typically with few competing males present. Killing those few competitors may secure valuable resources (both females and a host cadaver for nourishment of offspring). Non-IJ males develop in subsequent generations within a host cadaver, where the presence of many closely related male competitors increases the risk:benefit ratio of fighting. Thus, passage through the IJ stage primes males for enhanced aggression in circumstances where this is more likely to result in increased reproductive success. Fighting occurred between males developing in mixed-sex social groups, indicating that it is an evolved trait and not an abnormal response to absence of females. This is supported by finding high mortality of males, but not of females, across a range of population densities in insect cadavers. We propose that these nematodes, with their relatively simple organization, may be a useful model for studies of aggression.</p></div

Mortality (mean ± S.E.) of male <i>S. longicaudum</i> 24 h and 2–4 days after being placed in groups of 1–32.

1<p>Males were reared separately in hanging drops each inoculated with one infective juvenile before being placed in groups.</p

Fighting nematodes.

<p>Fighting in <i>Steinernema longicaudum</i> in a drop of insect haemolymph <b>A</b>. A male wrapped around the tail end of another male (the victim). The victim is moving rapidly at this stage, resulting in blurring of the image. <b>B</b>. The same pair ten minutes later. Here, the victim has slowed movement and is paralysed. Scale bar: 1 mm.</p

Mortality (mean ± SE) of <i>S. longicaudum</i> males and females developing together for 4–5 days in hanging drops of insect haemolymph inoculated with infective juveniles.

<p>Mortality (mean ± SE) of <i>S. longicaudum</i> males and females developing together for 4–5 days in hanging drops of insect haemolymph inoculated with infective juveniles.</p

Time course of killing in IJ-derived males.

<p>Percentage of pairs of male <i>Steinernema longicaudum</i> in which one male was either paralysed or dead at various times after the males were placed together; N = 36 pairs. None of the 36 single male controls was paralysed or dead after 24 h.</p

Developmental pathway affects killing.

<p>Effect of developmental pathway on fatal fighting in <i>Steinernema longicaudum</i>. Percentage of pairs in which at least one male was paralysed or dead 24 hours after they were placed together. Differences between the IJ and non-IJ pathways significant at <i>P</i><0.001 (chi-square, 1 d.f. = 41.049 for dead, 61.016 for total affected (paralysed or dead). Numbers on the bars are numbers of pairs. A maximum of 3% of single males suffered paralysis or death, significantly different to pairs for IJ (chi-square  = 34.239, 1 d.f., <i>P</i><0.001), but not for non-IJ (chi-square  = 2.064, 1 d.f., <i>P</i> = 0.151)</p

Effect of competitor density on killing in vivo.

<p>Percentage mortality (mean ± S.E.) of first generation adult males and females of the nematode <i>Steinernema longicaudum</i> in cadavers of the wax moth <i>Galleria mellonella</i>, with varying density, classed by number of males found in each cadaver. The number above the bar is the number of cadavers in each class.</p