Intense harvesting of eastern wolves facilitated hybridization with coyotes: Rutledge et al. (2011)

Eastern wolf (Canis Lycaon) photographed at Brule Lake

 in Algonquin Provincial Park. Photograph by Michael Runtz.

Abstract

"Despite ethical arguments against lethal control of wildlife populations, culling is routinely used for the management of predators, invasive or pest species, and infectious diseases. Here,we demonstrate that culling ofwildlife can have unforeseen impacts that can be detrimental to future conservation efforts. Specifically, we analyzed genetic data from eastern wolves (Canis lycaon) sampled in Algonquin Provincial Park (APP), Ontario, Canada from 1964 to 2007. Research culls in 1964 and 1965 killed the majority of wolves within a study region of APP, accounting for approximately 36% of the park’s wolf population at a time when coyotes were colonizing the region. The culls were followed by a significant decrease in an eastern wolf mitochondrial DNA (mtDNA) haplotype (C1) in the Park’s wolf population, as well as an increase in coyote mitochondrial and nuclear DNA. The introgression of nuclearDNA from coyotes, however, appears to have been curtailed by legislation that extended wolf protection outside park boundaries in 2001, although eastern wolf mtDNA haplotype C1 continued to decline and is now rare within the park population. We conclude that the wolf culls transformed the genetic composition of this unique eastern wolf population by facilitating coyote introgression. These results demonstrate that intense localized harvest of a seemingly abundant species can lead to unexpected hybridization events that encumber future conservation efforts. Ultimately, researchers need to contemplate not only the ethics of research methods, but also that future implications may be obscured by gaps in our current scientific understanding."

Map of Ontario, Canada. Dark gray area is Algonquin ProvincialPark (APP) where samples were collected for this study over a 43-year period. Other samples used in this study include gray wolf–eastern wolf hybrid animals from northeastern Ontario (NEON; checkered oval) and coyote–eastern wolf hybrid animals from south of APP Park along the Frontenac Axis (FRAX; gray oval).

Introduction

"[…] In recent years, the impact of human-caused mortality on the genetic composition of populations has received much attention because exploitation fosters evolutionary alterations that may increase the risk of extinction, induce rapid evolution of life-history traits, increase hybridization, and impact behavioral dynamics in kin-based social groups. There is little doubt that intense harvest, especially over long time periods, results in genetic alterations that can be detrimental to populations and ecosystems. […] Molecular genetic monitoring of populations over time is a powerful approach to facilitate an understanding of genetic changes in populations impacted by harvesting, particularly for small populations of threatened species.  Interpreting genetic data within the context of demographic history is also critical to accurately explain genetic change. Wolves across North America have been subjected to intense eradication efforts that have limited their genetic variability and evolutionary potential, promoted coyote (C. latrans) expansion eastward, and increased coyote hybridization with eastern wolves (C. lycaon) and red wolves (C. rufus). [..] Unlike gray wolves in the west, eastern wolves readily hybridize with coyotes, and it has been suggested that high mortality of APP wolves could lead to gene swamping by coyotes that are ill-suited to occupy the niche of an apex predator and exert substantial top–down limitation of large ungulate prey species (i.e., deer and moose) due to their small size. If intense harvesting of eastern wolves in APP results in increased hybridization with neighboring coyote populations, trophic interactions may be decoupled or otherwise altered. There has also been some suggestion that disruption to pack social structure associated with harvest pressure and breeder loss could increase eastern wolf hybridization with coyotes when harvest occurs during breeding season. 

Assumed model of population and demographic history for eastern wolves and coyotes in eastern North America.

[…] Although wolves in APP, Ontario Canada (Fig. 2) are amorphologically and genetically differentiated group of approximately 200–300 eastern wolves that share a common evolutionary lineage with coyotes and red wolves, prior to the year 2000, they were thought to be a gray wolf subspecies (C. lupus lycaon) that at the time was abundant across Ontario. Within the park, wolves have survived a long history of control efforts dating back to the park’s establishment in 1893. […]Although wolf harvest in the first half of the 20th century presumably impacted the population size and altered the original genetic makeup of wolves within the park, the timing of the research culls in the mid-1960s is important because it occurred at a time when coyotes were becoming well established in the area. Prior to the 1960s, introgression from coyotes may have occurred, but was likely limited because the first coyote confirmed in southern Ontario was recorded in Thedford, Lambton County in 1919  and densities near APP would have been relatively low until the beginning of the 1960s when coyote populations expanded rapidly north, east, and south in response to new habitat made available through land clearing and wolf extirpation. […] To explore the long-term impacts that wildlife culls can have on conservation, we analyzed genetic data acquired from eastern wolf samples collected in APP over a 43-year period (1964–2007), and interpreted genetic changes within the context of wolf and coyote demographic history in and around APP. Ultimately, this research demonstrates that although intense localized killing of an apparently abundant species may seem innocuous under the accepted scientific framework of the time, it may have lasting, and unforeseen, conservation implications. […]

Number of Canis clusters inferred from six autosomal microsatellites. Top figure shows mean log probability of the data (dashed line) and the second-order change of the likelihood function ([1]K) (solid line) as a means of inferring the number of clusters in the data. Arrows indicate “population” divisions, APP = Algonquin Provincial Park. At K = 2, the major division between Old World evolved animals (gray wolves) and New World evolved animals (eastern wolves and coyotes) occurs. At K = 3, eastern coyotes separate and APP animals from all three time periods cluster together. K = 4 hints at a division within Algonquin animals, but this division is difficult to interpret biologically and should be treated with caution. Overall, K = 3 is the most likely number of clusters.

Simulations

Coalescent simulations generate the genomes of individuals, moving backwards in time, under a defined demographic scenario with the assumption that the coalescent process for neutral markers will be determined by the population and demographic history. Using coalescent simulations, one can determine the distribution of genetic summary statistics under a given demographic scenario and determine if the observed data fall within or outside of the expected distribution. […]

Proportional representation of wolves in APP in the three different time periods assigned in Structure as (A) Algonquin Provincial Park (APP; Q ≥ 0.8 to APP); (B) influenced by hybridization with eastern coyotes from Frontenac Axis (APP-FRAX; 0.8 ≥ Q ≥ 0.2 to FRAX); (C) strongly assigned to FRAX (FRAX; Q ≥ 0.8 to FRAX); (D) influenced by hybridization with gray wolf–eastern wolf hybrids from northeastern Ontario (APP-NEON; 0.8 ≥ Q ≥ 0.2 to NEON); (E) assigned with Q ≥ 0.2 to all three populations (APP-NEON-FRAX). HH64–65 = Historic Harvested samples collected between 1964 and 1965; CH87–99 = Contemporary Harvested samples collected between 1987 and 1999; CP = Contemporary Protected sampled collected between 2002 and 2007.

Discussion

[…] Killing of wolves during the mid-1960s in APP appears to have influenced the genetic composition of the Park’s wolf population. Although researchers at the time could not have predicted these outcomes, it seems likely that extensive culling of wolves prompted the few remaining wolves in the Park to mate with individuals from the expanding coyote population. The subsequent decline of an eastern wolf mtDNA haplotype and introgression of coyote mitochondrial and nuclear DNA correlates well with the demographic history of the two species, and coalescent simulations suggest these outcomes were unlikely in the absence of harvest pressure. […]

[…] Above all, our results demonstrate that intense localized harvesting of species thought to be numerous and widespread can have unexpected outcomes that threaten conservation of species and naturally functioning ecosystems. The advanced molecular genetic techniques now used for studying wildlife populations were unheard of in the 1960s and no one could have predicted the impacts that such an experimental design could have on a population. Although the research methods used in the 1960s would fail to meet current ethical guidelines, targeted culling is still common practice for managing wildlife under various scenarios. For example, lethal control of gray wolves (C. lupus) is currently used to increase the size of ungulate populations in Alaska, USA, and in Alberta, Canada where both total wolf harvest and areas of intense harvest (>45 wolves/1000 km2) have increased over the past 22 years. Similarly, lethal methods are routinely used for coyote control, with intense “spatially clumped” harvest suggested as more effective than random removal across a broad spatial scale. Coyotes are generally regarded as vermin, and wolves are often perceived as a major threat to ungulate populations; both of these view points were similarly applied toward wolves in APP prior to 1965.

Our results suggest the potential for ecological assumptions to be incomplete and that culling and other seemingly harmless, invasive methods, even when applied to abundant “pest” species, may have unexpected, lasting conservation implications. Whether for the purpose of game species management, protection of endemics, population size estimates, or collecting basic ecological knowledge, exploring nonlethal alternatives could minimize unanticipated impacts to animal populations and thus reduce the burden on wildlife managers. By following guidelines and principles of ecological ethics as outlined by a growing number of scientists, sampling methods are less likely to result in unanticipated negative impacts. In this way, we can avoid leaving behind a legacy of complications for future conservation biologists and wildlife managers.

Intense harvesting of eastern wolves facilitated hybridization with coyotes: Linda Y. Rutledge, Bradley N. White1, Jeffrey R. Row1 & Brent R. Patterson: (2011) http://bit.ly/Q9FyFM Ecology and Evolution Volume 2, Issue 1, Article first published online: 23 Nov. 2011. (Publicado por: http://onlinelibrary.wiley.com/ )