ited by resources and can increase at the maximum growth rate). The goal of maximum-sustainable yield is to balance mortality with productivity at the maximum intrinsic rate of population grown. While this approach is considered appropriate to maximize yields, there are additional factors that need to be considered when identifying the impacts of harvest on 
wild animal populations. In particular, harvest may be leading to ‘unnatural’ selection in animal populations and this may have important evolutionary and conservation implications. The impact of harvest has been observed in aquatic and terrestrial systems. Atlantic cod showed dercresed size and age at maturation in response to harvest (Olsen et al. 2004, Swain et al. 2007) and the percentage of tuskless elephants increased in response to harvest (Jachmann et al. 1995).
Human harvest of wild animal populations is almost always non-random. It is often the case that individuals are selectively harvested from the population based on some desirable phenotypic trait. If this phenotypic trait is heritable, significant evolutionary change could arise due to harvest. Allendorf and Hard (2009) indentified several traits that are to be affected by harvest (see Table 1. Traits likely to be affected by unnatural selection in harvested populations). Harvest of wild populations can result in a variety of direct and indirect effects on populations that can influence the viability and sustainable yields drawn from the population (see Figure 1. Human harvest can have a variety of direct and indirect genetic effects on populations). Allendorf et al. (2008) identified three types of genetic change that can occur as a result of harvest: 1) alteration of population subdivision, 2) loss of genetic variation, and 3) selective genetic changes. Below, I briefly highlight each of these types of genetic change.
Alteration of Population Subdivision: Populations are often made up of reproductively isolated subpopulations, but harvest occurs within the population as a whole. Some subpopulations may have genetically desirable traits (e.g., larger body size) that make them more prone to excessive harvest. If harvest is disproportionately directed towards one subpopulation, that subpopulation is likely to go extinct. This has several important implications. The loss of one or more subpopulations will reduce the viability of the metapopulation. Extinction of local subpopulations can reduce the overall genetic diversity in a population and contributes to the loss of unique genes that are adapted to local environments. Loss of genetic diversity can reduce the ability of the population to respond to environmental change. Furthermore, reduction of local populations can increase immigration, leading to swamping of locally adapted genes and possibly outbreed depression.
Loss of Genetic Variation: Overharvest can result in substantially decreased population size. As a result, the population may go through a genetic bottleneck and much of the genetic diversity in the population could be lost. Harvest may also specifically target a specific sex; as a result the effective population size is substantially reduced. Species with a lower effective population size lose genetic diversity at higher rates. Furthermore, if certain genes are responsible for the phenotypes that make individuals susceptible to harvest, these genes can be removed from the population over time due to ongoing harvest pressure.
Selective Genetic Changes: This type of genetic change is similar to ‘artificial selection’ in domestic breeding. Several studies have indicated changes in phenotypic traits of populations following extensive human harvest (see Table 2. Examples of phenotypic changes that could have resulted from exploitative selection). The impacts of selective harvest can be seen in terrestrial systems and aquatic systems. However, in most of these studies it has been extremely difficult to determine if the phenotypic changes are attributable to actual genetic changes or other factors (e.g, abiotic factors).
Trophy hunting of bighorn sheep provides a practical case study for assessing the impacts of selective harvest of heritable phenotypic traits (Coltman et al. 2003). Hunting bighorn sheep is a popular recreational hunting opportunity in much of North America. Over the course of 30 years, 57 rams were harvested from a sheep population in Alberta, Canada using a 4/5th curl length restriction. Most of the rams that were harvested were less than 8 years old. Bighorn rams add most of their horn length between the ages of 2 to 4 years, and the probability of a ram being shot before the age of 6 years is correlated with the horn growth during the age of 2 to 4 years. Hunters were selecting rams with high “breeding value” (twice the expected deviation of an individual’s offspring phenotype from the population mean owing to the additive effect of the offspring’s inherited genes). In other words, the rams that grew quickly and had large horns at a young age had the highest reproductive fitness and were most likely to be killed by hunters. Trophy rams (i.e., rams with large bodies and horns) had genes that promoted rapid horn growth and large body size, which was correlated with increased reproductive fitness. However, the same genes that increased reproductive fitness were also contributing to the likelihood the individual would be harvested by a hunter. As a result, individuals that would be ‘most fit’ under natural selection were being removed from the population prior to being able to breed. The selective pressure being inflicted by hunting was in the opposite direction that would be expected by natural selection. This ongoing selective pressure led to average breeding value for horn length and weight declining over time in the population (see Figure 3. Changes in the mean breeding value of cohorts born between 1967 and 2002). This was evidence of microevolutionary selection occurring in the population – the value of having a large body size and large horns was being lost. Smaller rams with smaller horns were now conducting the majority of the breeding in the population.
In effect, hunters were removing the rams with the highest reproductive fitness before they were able to successfully breed, removing genes from the population that confer with early rapid growth of horn size and body weight. Over time, this process resulted in decreased trophy ram size (see Figure 2. Observed changes in mean weight and horn length and in the population size from 1972 to 2002), degraded the recreational value associated with the hunt and the number of trophy rams available for harvest. Perhaps of bigger concern is the potential loss of genetically correlated traits. For example, the selective harvest of the fastest growing and largest rams may result in decreased body size in future generations. Body size is often positively correlated with disease resistance and survival in many ungulates. As a result of decreased survival and disease resistance, the viability of the population may be reduced and the population will be more prone to extinction. To mitigate the potential negative effects of long-term selective harvest of fast growing rams, the authors proposed that a full curl harvest restriction be implemented in this (and other) bighorn sheep populations. This restriction will allow the fastest growing rams to reach their peak breeding age (approximately 8 years old) before they are available for harvest. As a result, they will be able to pass on their genetic material prior to being harvested.
These results indicate that managers of wildlife and fisheries population need to consider the genetic and evolutionary impacts of harvest on wild animal populations. There are many unintended consequences associated with the harvest of wildlife and managers need to move beyond maximum sustainable yield management prescriptions to ensure the long-term viability and health of wild animal populations.
So the activities of the game hunters and fisheries impose artificial purifying selection upon populations, but instead of selecting against deleterious alleles, they are selecting against those that confer the greatest fitness to individuals. In terms of an adaptive landscape, this would not only limit a population to a local adaptive peak below maximum fitness, but reduce the level of the peak as allele frequencies within the gene pool are reduced without being replenished.
ReplyDeleteThis article really underlines the fragility of populations when influenced by unnatural forces.
Do you think a restriction on harvesting animals before they are mature enough to breed is enough? What other measures could be instigated?
Perhaps selective breeding programs to counteract the effects of harvesting?
I am not sure that restricting age at harvest is enough to remove the impacts. Another consideration is that the level of harvest likely needs to be limited. Another option is to not harvest every year, that way the larger individuals will get an opportunity to breed before they are harvested. Any harvest strategy that targets a certain size/age class will likely have impacts, but as long as managers are accounting for these potential impacts the overall impact should be minimized. Managers need to carefully consider all of the impacts of their harvest strategy because there could be unintended consequences.
ReplyDeleteSelective breeding could be an opportunity to increase genetic diversity, but this is an unlikely scenario. Ex situ breeding is terribly expensive and is usually reserved for only the rarest or critically endangered species. Most harvestable populations are not threatened or endangered so they would likely not be considered for ex situ breeding given there are greater concerns. Furthermore, most conservation is in situ because we want to allow populations to persist in their natural habitat.
As a potentially better alternative, using big horn sheep as an example, would be to bring in sheep from adjacent populations that have not been overharvested and release them into the population to increase genetic diversity. After some genetic diversity has been restored a altered management regime would be needed to prevent similar outcomes in the future.
It really hurts me to see or hear that this is happening. The case you mentioned for rams and the case of hatcheries are just two examples. Is it possible that we can avoid these measures entirely?
ReplyDeleteI know that fish hatcheries provide more fish, but like you mentioned, the fish hatcheries decrease the genetic variation of the population as a whole. Also, organisms that are bred and born in close proximity to humans can also be detrimental. Fish in hatcheries flock toward humans (because they are used to being fed) instead of fleeing or seeking refuge. So even though there are larger numbers of fish, more fish may not even make it back to their original streams due to predation.
You have have a table (table 1) that has a list of remedies to the problems that the human harvest poses. However, I believe that many of those remedies may not be upheld enough to where they can truly make a difference in the population that is being harvested. There are obviously individuals that bend the rules or break them, and this could still lead to problems in populations that are human harvested.
Are there any other measures that could be taken? Even if we consciously make efforts to avoid issues with human harvesting, isn't our mere presence enough to harm populations of organisms, including humans? The population of humans is continuing to increase and it seems that there may be no way to sustain our population without always having a negative affect on other organisms (especially the ones that we use for food or for recreational purposes).
What are some potential alternatives to human harvest, hatcheries, breeding, etc.?
Its funny that the traits that trophy hunters are interested are being eliminated by the artificial selection being put on the bighorn sheep.
ReplyDeleteI wonder if along with the restrictions on the circle length of the horn and with the alternating the hunting seasons if the use of hunting ranches will also relieve the selection pressures on big horn sheep caused by humans. Also you mention the study of the Atlantic Cod in which the age of sexually maturity in the Cod has gone down. However there is no mention to any study of this happening with the sheep. Has there been any study done on the age and size of sexual maturity in the bighorn sheep?
This post made me think about the size limitations in commercial and recreational fishing. I know that size limits are put into place to allow enough time for development in fish, but it seems to me that having size limitations only reinforces smaller individual having a disproportionate level of the matings. I wonder if size restrictions on bigger individuals as well would do anything to stop this directional selection.
ReplyDeleteOver-harvesting just reinforces more over-harvesting as individuals evolve to be small. This just leads to more harvesting to meet the quota. It really just boils down to randomly harvesting individuals in a way that is sustainable and being flexible enough to find substitute goods when a population drops below a certain threshold.
This is an interesting phenomenon to read about because it is an aspect of commercial and trophy harvest that had never occurred to me. I had only ever heard of the negative effects of over harvesting and assumed that size and sex restrictions were a good solution to the problem. However, after reading this article and considering the evolutionary concepts of BI445, this issue seems to be more obvious.
ReplyDeleteIt seems like adding age restrictions were to the current harvest restrictions would be an effective cure for the problem. However, in many species affected by this problem, it seems like judging age would be a difficult task for the hunter. For example, in commercial fishing how would fishermen be able to judge age of fish in the catch? It seems like this would be a difficult task and would have major economic impacts on the industry.
It is concerning to me that this is occurring and seems that in most cases the most obvious solution, selecting individuals for harvest that are at an age where they have already made their genetic contribution to the population, would be nearly impossible to perform. It makes me wonder if there are any other restrictions that could be imposed to remedy the problem.