Authors: Olivia Davis, Lauren Spangler and Phil McNamara
Biology Department, University of Washington, Seattle, WA 98195
Pheromones are chemical substances that serve especially as social stimuli to other individuals of the same species for one or more behavioral responses (Karlson & Luscher, 1959). While it was once thought that only eukaryotes were able to use chemical cell signaling, it was found to also occur in bacteria (Miller & Bassler, 2003). Studies have shown that species ranging from bacteria to humans (Radulescu & Mujica-Parodi, 2013) can use chemical signals in a variety of ways, including as a sexual attractant (Katona, 1973), for establishing territory (Traniello, 1989), as well as for chemical alarm cues (Meuthen, Baldauf, &Thünken, 2015). How do different species use pheromones and how do other members of the species respond effectively?
One way many species have been able to use pheromones to their advantage is through alarm cues. In the presence of a predator, a chemical alarm cue can be produced by the sender (the prey), effectively warning others, particularly members of the same species, of the present danger. However, the sender of the signal may not survive (Meuthen, Baldauf, & Thünken, 2015). What is the evolutionary benefit? How did chemical alarm cues evolve? One popular scientific hypothesis for this advantage is the kin selection hypothesis. The kin selection hypothesis states that by sending an alarm cue to kin, kin will respond, ensuring the sender’s genetic material will be passed on to future offspring, even if the sender does not survive. For example, Richard Karban and colleagues found that plant’s kin respond more effectively to chemical signals than non-kin (Karban, Shiojiri, Ishizaki, Wetzel, & Evans, 2013). Additionally, Eastern chipmunks send out alarm calls in the presence of a predator to increase their inclusive fitness by potentially saving their kin from such predators(Burke da Silva, Mahan, & da Silva, 2002). Denis Meuthen, Sebastian A Baldauf, and Timo Thünken attempt to shed further light on this topic by using the cichlid fish species Pelvicachromis taeniatus, to test the effects of kin alarm cues vs non-kin alarm cues on the behavior of these fish (Meuthen et al., 2015).
Alarm cues are not just found in P. taeniatus, but throughout many species of fish. Many coral fish species use chemical alarm cues in the presence of predators (Mitchell, Cowman, & McCormick, 2012) as do rainbow trout, which may be important in teaching hatchery fish to recognize chemical alarm cues (Brown & Smith, 2011). The common link between most alarm signals in fish seems to be that the chemical alarm cue is transmitted when the fish is injured. Minnows have been shown to have a chemical in their skin cells that is released when the cells become damaged (Wisenden, Vollbrecht, & Brown, 2004). What has yet to be completely understood, however, is why such a mechanism evolved. Some studies have reported that releasing chemical alarm cues has a direct benefit to the sender. For example, in a study by Doug P. Chivers and colleagues, they suggested that the alarm cells in the skin of fishes may be able to protect the fish against pathogens, parasites, and UVB radiation after injury (Chivers et al., 2007). Yet the kin selection hypothesis has remained a possibility as well.
To explore further, do fish respond better to alarm cues from relatives? Discovering the answer to this question may help further our understanding of why chemical alarm cues evolved, as it seems that the sender of a chemical alarm cue has low chance of survival and may receive little direct benefit in emitting any sort of signal at all. Additionally, alarm cues are expensive to produce, which brings even more question to their possible fitness benefit. How did a mechanism with so little benefit to the sender of the alarm cue develop and evolve over time? Understanding what an individual could gain from emitting chemical alarm signals is vital to understanding the evolution of chemical signaling. In their study, Meuthen and colleagues offer further insight into this puzzling question.
The nature of alarm signals provided a problem for evolutionary biologists. Upon predation, certain fish phylogenies release a chemical substance into the water called “schreckstoff,” which serves as an alarm signal for other nearby prey (Irving and Magurran, 1997). Chemical signals released into the water disperse broadly and it is impossible for only the relatives of the deceased to get a benefit. Thus when it comes to intra-species competition, producing schreckstoff appears to provide no advantage. In 2012, Denis Meuthen and his research team looked at a possible solution to this problem: that fish can sense the signals of their kin and respond to them in a way that non-kin cannot. This would give a greater survival rate to relatives of the dying fish in a predatory attack and increase its fitness.
In order to assess the hypothesis that fish respond better to the signals of their kin, Meuthen and his colleagues experimented on P. taeniatus, a cichlid known to respond to chemical alarm signals. Schreckstoff was generated by euthanizing cichlids and grinding them with a mortar and pestle, simulating a lethal predation event. Female cichlids were then exposed to normal water, water containing an alarm signal from a related fish, or water containing a signal from an unrelated fish. Their movement was monitored using a video camera, as the response by cichlids to a potential predator is to remain still. Although movement decreased in the presence of the schreckstoff, no significant difference was observed in the response to kin vs. non-kin signals (p = 0.63). Fish were also measured for standard length and weighed for body mass, which did not differ between the three treatments. From these results the authors concluded that cichlids cannot distinguish kin from non-kin signals and that the kin selection hypothesis does not fully explain the evolution of schreckstoff.
The fact that cichlids cannot differentiate between alarm signals does not rule out the role of kin selection, but it does necessitate alternative hypotheses. One such idea was developed by Douglas P. Chivers et al., who found that schreckstoff production was not stimulated by increased predation but instead by skin parasites and UV radiation. The idea of evolutionary traits taking on a secondary function is known as exaptation and is well established. Feathers most likely evolved as an efficient form of heat regulation before their use in flight (Barve and Wagner, 2013). The function of schreckstoff as an alarm signal could have evolved later, with its fitness value coming from its immune function. Another idea is that because P. taeniatus have behaviors of kin-shoaling (Hesse and Thünken, 2014), kin selection could still be at work because the receivers that get the benefit from the alarm cue are kin of the sender. Since these fish live in kin groups, this means that most of the time the fish that sends an alarm cue will be sending the cue to kin, and therefore increases the inclusive fitness of the sender.
Kin selection theory has been upheld by several experiments across many different species. However, Meuthen and colleagues’ (2012) experiment contrasts these previous findings in that they found that P. taeniatus did not have different responses between kin and non-kin alarm cues. However, the alarm cues from kin and non-kin alike did decrease the activity of prey which would increase their survival in the presence of visual predators. The authors explained that their results show no direct or indirect link between alarm cues and kin cues, but this does not mean kin were not recognized in the fish since kin could have been recognized during trials. The authors argued that because of the behaviour of P. taeniatus such as kin-shoaling (Hesse and Thünken, 2014) and their ability to identify and live in kin-shaped groups (Ward and Hart, 2003), kin discrimination in alarm cues did not have to evolve in P. taeniatus . Since P. taeniatus already lives and mostly associates with kin it wasn’t needed for alarm cues to have a stronger response from kin because kin were already receiving benefit from alarm cues due to their close association with each other. So, as the author suggest kin selection theory may still be at work here but through more indirect means then other experiments have shown.
Future questions that should be considered for this topic would be if P. taeniatus schreckstoff is possibly an exaptation, what were the evolutionary mechanisms to drive schreckstoff as an alarm cue? Another question related to the previous one would be: what are the direct benefits of schreckstoff as an immune enhancing mechanism? Also, could the evolution of kin-shoaling and other behaviours of P. taeniatus be an indirect form of kin selection when alarm cues are dispersed? Further research should be concluded to answer these questions and to determine the direct costs and benefits to senders and receivers of alarm cues. However, Meuthen and colleagues (2012) presented a new way to look at the kin selection theory, which is that the direct mechanisms may not be present but indirect factors can play a role in ensuring kin survivability and thus indirectly increasing the sender’s fitness. Further, they demonstrated that evolution is complex and that all the mechanisms of it are still not completely known. The broader implications of these findings is that other species of vertebrates, plants, and invertebrates that use alarm signals and pheromones to communicate to other members of it’s species may be using these chemical signals for more than one purpose. It might be possible for species that form tight living groups with kin and regularly use pheromones and chemical signaling to communicate with each other, that they may as well be using their alarm signals when a predator is near as an indirect form of kin selection, similar to Meuthen and colleagues experiment (2012). This would mean that the research into chemical signaling between species and how these signals evolved needs to be further examined with the thought of indirect kin selection in mind. As Kocher and Grozinger (2011) described, “Elucidation of the factors that led to the evolution of complex chemical communication systems is challenging: it requires characterization of both proximate and ultimate factors underlying pheromone production and response” (p. 1271). Chemical signaling is highly complex and great care and consideration must be taken into researching how these mechanisms evolved not only in P. taeniatus but in the countless number of organisms that use pheromones and chemical signaling.
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