Antagonism is an interaction between two populations that positively affects the fitness of one population and negatively affects the fitness of the other population. The two most common and commonly investigated antagonistic relationships are predator-prey and host-parasite. The predator and parasite gain sustenance while the prey and host either die or suffer. An interaction is typically labeled predator-prey if it is characterized by a short period of interaction and prey death. Host-parasite interactions are characterized by a longer period of interaction that causes host damage and may or may not eventually lead to death. The parasites are usually bacteria, viruses, or other small organisms.
Under selection induced by antagonistic interactions, theory predicts that in most cases coevolution proceeds in a direction such that the prey (or host) tries to genetically 'escape' or defend against the interaction, while the predator (or parasite) tries to 'track' this escape or counter the defense. The idea that constant evolutionary change is necessary in antagonistic relationships in order to simply maintain population fitness level is called the Red Queen Hypothesis. There are two major ways in which this constant coevolution can occur: an 'arms race' between corresponding predator-prey quantitative traits and coevolutionary alternation, which results from frequency-dependent selection.
For parasites and their hosts, there is a third option. Although parasites need to exploit their prey, they do not benefit from over-exploiting their prey. If the host dies too quickly, this can affect a parasite's ability to survive, reproduce, and spread. Therefore, it has been observed that parasites can evolve to be less virulent, causing less damage to the host, thereby relaxing selection on the host for parasite defenses. This coevolutionary consequence is called attenuation, and has been studied extensively for its role in disease and parasite evolution.
The following example is based on the research of Brodie et al. Suppose that a lizard has a genetically controlled poison concentration of 0.001%, and its major predator, a snake, has a genetically controlled resistance of 0.002%. Then, in response the lizard population may evolve in such a way that the poison concentration exceeds predator tolerance if it does not detract too much from its reproductive success. The snake population might then reciprocally respond by developing a poison tolerance above the lizard population's poison levels. This coevolu-tionary result is referred to as an evolutionary arms race or coevolutionary escalation. It is limited by physical constraints, that is, the capability must exist. In addition, the defense and counter-defense must increase or maintain the net fitness of the population, so it cannot impose too much cost on the reproductive system or other systems which contribute to the fitness of the population.
If the mechanism for genetic escape causes the prey or host species to experience a species radiation, that is, several new species quickly evolve, then that process and the resulting tracking radiation of the predator or parasite is called 'escape and radiate'. It has been observed that speciation rates are higher when parasites are part of the ecological interactions that a population experiences. The next section discusses coevolutionary research and results of the predator-prey relationship between lodge-pole pine and red crossbills in the northwest United States.
One well-known example of coevolution as a result of antagonism is the case of the Rocky Mountain lodgepole pine (Pinus contorta latifolia) and the red crossbill (Loxia curvirostra complex). The red crossbill feeds on the pine-cone seeds of the lodgepole pine, making the red crossbill-lodgepole pine interaction an antagonistic predator-prey interaction. Over the course of this relationship, where the ranges of these two populations overlap, the red crossbill has evolved a bill adapted to feeding on the lodgepole pine. In response, the pinecone shape of the lodgepole pine has evolved to counter the red crossbill predation.
In some areas, the red squirrel is also a major predator of lodgepole pinecone seeds. In these areas, lodgepole pinecone shape has also evolved in response to the squirrel predation, resulting in a distinctly different pinecone shape. This illustrates how one population can coevolve in response to one or a combination of two different antagonistic relationships. As expected, in response, red crossbills that forage in geographic areas where the red squirrels also forage have a different beak shape than red crossbills with ranges that do not overlap with red squirrels. Current investigations center around how the antagonistic interactions in different geographic areas and their correspondingly different responses can promote speciation among crossbills (see also the section entitled 'Geographic mosaic of coevolution'). For a more in-depth discussion on this predator-prey system see the 'Further reading' section.
When predator-prey (or host-parasite) states alternate as a consequence of antagonistic interactions, it is called coevolutionary alternation. For example, consider a fight or flight mechanism in a prey species and a corresponding strength or agility trait in the predator species. If prey that fight are the most plentiful, the predator population might evolve to consist mostly of strong and stocky predators to win encounters. In response, the prey population might decide to choose flight instead, outrunning the stocky predators. Now the predator population shifts so that its population will consist mostly of light and agile predators to chase the fleeing prey, now the most plentiful prey available. These predator-prey frequency oscillations are the coevolutionary result of positive frequency-dependent selection due to an antagonistic interaction.
Because genotype and phenotype frequencies can oscillate, it is important not to draw quick conclusions based on a snapshot of evidence. In some cases, populations at different points of their cycling frequencies may appear to be different species or subspecies, because of the different allele frequencies found when sampling the populations. Current mathematical models explore the coevolutionary consequences of weak migration between subpopulations that experience frequency cycling behavior. The differences in the intrinsic cycle due to heterogeneity of environments may play a huge role in coevolutionary dynamics (see the section entitled 'Geographic mosaic of coevolution').
speciation. Below is a sampling of some types of mixed ecological interactions and their coevolutionary consequences.
Before Emerson and Kolm's Nature article, Christensen, etal. proposed the Tangled Nature model. This model set up hundreds of populations with 64 interacting loci which interacted in a randomly pre-assigned way, with either positive or negative results for each interacting population, and also included density dependence and mutation. These interactions lead to alternating periods of transition and stasis. During the shorter periods of transition, some species go extinct and new species arise. Then during the longer stasis periods, the species form a stable community. One major contribution of this model was to show that ecological interactions alone play a huge role in evolutionary dynamics, helping to account for periods of stasis and transition as well as speciation and extinction events. The approach, borrowed from statistical mechanics, also introduced a new mathematical model of complex ecological interactions. The Tangled Nature model demonstrates the power of modeling to generate evolutionary theory, and the need for data to validate or challenge this theory. With so many conjectures on the causes of biodiversity, studies like that of Emerson and Kolm coupled with mathematical models like that of Christensen et al., are important to move forward theoretical ecology and evolution.
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