Recovery and genetics of Mexican wolves: a reply to Hedrick et al.

IF 1.9 3区 环境科学与生态学 Q3 ECOLOGY Journal of Wildlife Management Pub Date : 2025-02-19 DOI:10.1002/jwmg.70005
Matthew J. Clement, John K. Oakleaf, James R. Heffelfinger, Colby Gardner, Jim deVos, Esther S. Rubin, Allison R. Greenleaf, Bailey Dilgard, Philip S. Gipson
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In support of this recovery strategy, we recently evaluated inbreeding depression in wild Mexican wolves in Arizona and New Mexico, USA, from 1998 to 2022 (Clement et al. <span>2024</span>). Our analysis did not detect any statistical association between inbreeding coefficients in a pack, as estimated from the Mexican wolf pedigree, and the number of pups surviving to 9 months (hereafter, recruitment). Hedrick et al. (<span>2025</span>) provided comments on our work, concluding that Mexican wolves “have shown inbreeding depression” and recommending that Mexican wolves hybridize with northern gray wolves (<i>C. l. occidentalis</i>) to induce genetic rescue. Here, we provide our perspective on inbreeding depression, genetic rescue, and other issues raised by Hedrick et al. (<span>2025</span>).</p><p>Hedrick et al. (<span>2025</span>) write rather definitively that Mexican wolves “have shown inbreeding depression.” This statement seems to be based on a combination of a prior expectation that low genetic diversity invariably leads to inbreeding depression and some older studies of Mexican wolves, but the current evidence does not support their claim with regard to recruitment in wild Mexican wolves.</p><p>Mexican wolves are descended from 7 founders, so they are highly inbred, which increases the risk of genetic problems. However, many endangered species have experienced genetic bottlenecks, yet some species, including some wolves, have not experienced inbreeding depression (Crnokrak and Roff <span>1999</span>, Kalinowski et al. <span>1999</span>, Brzeski et al. <span>2014</span>, Gooley et al. <span>2017</span>, Powell et al. <span>2023</span>) and some have experienced robust post-bottleneck population growth (Harding et al. <span>2016</span>). Because inbreeding coefficients do not consider the relative occurrence of deleterious alleles in the founders or standing population, inbreeding alone does not establish inbreeding depression. Hedrick et al. (<span>2025</span>) also point to syndactyly as evidence of inbreeding depression; however, they did not support this assertion with any evidence or citations.</p><p>While some early studies reported inbreeding depression in Mexican wolves, our recent paper represents the most current and best available science for wild wolves. For example, Fredrickson and Hedrick (<span>2002</span>) reported inbreeding depression in the body sizes of captive wolves, but this is a relatively indirect measure of fitness, compared to our analysis of recruitment in wild wolves. In addition to analyses of captive wolves, Fredrickson et al. (<span>2007</span>) reported inbreeding depression in the maximum number of wild Mexican wolf pups observed during summer. However, our recent analysis benefited from a much larger sample size (352 pack-years vs. 39 pack-years), more timely litter size counts (within 6 weeks vs. within several months), and a more comprehensive fitness metric (combining litter production, litter size, and survival vs. summer pup counts). This is not a criticism of Fredrickson et al. (<span>2007</span>) because they used the best data available at that time, but our recent analysis produced more reliable inferences for recovery actions because of the advantages listed above.</p><p>Hedrick et al. (<span>2025</span>) recommend hybridizing with northern gray wolves as a remedy for inbreeding in Mexican wolves. However, hybridization would threaten the integrity of Mexican wolves, bringing clear risks and uncertain benefits, all at a time when the available evidence indicates genetic rescue is not necessary. In recommending hybridization, Hedrick et al. (<span>2025</span>), do not address several important considerations, including the legal status of Mexican wolves as a distinct taxonomic entity (USFWS <span>2015</span>), the risk of genetic swamping (Edmands <span>1999</span>, Gippoliti et al. <span>2018</span>, Odell et al. <span>2018</span>), and recent progress towards recovery goals (USFWS <span>2024</span>).</p><p>Mexican wolves evolved a distinct genetic and phenotypic profile in Mexico and adjacent portions of the American Southwest, and they fill a unique ecological niche in their native habitats. Accordingly, the USFWS has designated Mexican wolves as a separately listed endangered subspecies (USFWS <span>2015</span>). Hybridizing with large, Canadian northern gray wolves, as proposed by Hedrick et al. (<span>2025</span>), would compromise the Mexican wolf as a distinct subspecies. Given the smaller body size, higher inbreeding, smaller pack size, and lower abundance of Mexican wolves, hybridization would create a risk of genetic swamping, in which unique portions of the Mexican wolf genome are lost (Odell et al. <span>2018</span>). Even if hybridization initially induces heterosis, in the long term, introgression of traits that evolved in Canada could lead to outbreeding depression, reducing the fitness of hybridized Mexican wolves in some southwestern habitats (Edmands <span>1999</span>, Edmands and Timmerman <span>2003</span>, Gippoliti et al. <span>2018</span>).</p><p>Hedrick et al. (<span>2025</span>) argue that hybridization is necessary because Mexican wolves “have shown inbreeding depression.” As discussed above, their claim rests on older, smaller studies (Fredrickson and Hedrick <span>2002</span>, Fredrickson et al. <span>2007</span>), while dismissing a larger and more current study that did not detect inbreeding depression (Clement et al. <span>2024</span>). Additionally, they do not address the fact that the wild population is currently thriving, which is not consistent with a population in need of genetic rescue. For example, the wild Mexican wolf population has averaged 14% annual growth since 2010, yielding a population that exceeded interim recovery goals by 67% just 5 years into the current recovery plan (USFWS <span>2024</span>). In addition, gene retention and mean inbreeding in wild Mexican wolves have been better than interim recovery targets (USFWS <span>2024</span>), indicating that current management is maintaining genetic diversity without hybridization. Hybridization with northern gray wolves given no demonstrable need would be an irreversible ecological experiment that could harm recovery of Mexican wolves.</p><p>Hedrick et al. (<span>2025</span>) critiqued our analysis of artificial food caches (which they call “supplemental feeding”). Food caching is a practice in which some denning wolves are provided food during some or all of the pup-rearing season (April to September). Food caches may be provided to wolves near ranches or residential areas to reduce conflicts with people, or to packs with foster pups with the intent of increasing pup survival. Inbreeding levels are not used to decide which packs receive food caches and packs with foster pups were excluded from our analysis. Hedrick et al. (<span>2025</span>) argue for estimating an interaction between inbreeding and food caches on the grounds that food caches may mask inbreeding depression. We fit a simpler additive model (which indicated that food caches increased recruitment) because estimating an interaction for an attenuating effect (i.e., food caches reduce the impact of inbreeding) requires large sample sizes (Sommet et al. <span>2023</span>). Even without estimating an interaction, we can assess the argument by Hedrick et al. (<span>2025</span>) logically. The overall association between inbreeding and recruitment was not significantly different from zero (Clement et al. <span>2024</span>). If, as Hedrick et al. (<span>2025</span>) hypothesize, recruitment in unfed packs was negatively associated with inbreeding, then recruitment in fed packs (which constituted 46% of packs) must have a positive association with inbreeding (to maintain the overall slope close to zero). But a positive association between inbreeding and recruitment is biologically implausible and not consistent with a hypothesis of masking. In addition, since 2019 the percentage of packs receiving food has been substantially reduced from that projected in the 2017 Recovery Plan, yet the population has surpassed interim abundance and genetic targets (USFWS <span>2024</span>). There is no indication that feeding is masking inbreeding depression.</p><p>Hedrick et al. (<span>2025</span>) also critiqued our handling of packs that did not produce litters, writing “Clement et al. (<span>2024</span>) only considered inbreeding in litters when there was one or more offspring.” Their statement is incorrect. We estimated the temporal trend in mean inbreeding coefficient only for successful litters (≥1 pup) because non-existent litters are not part of the population. However, our fitness metric, pup recruitment, included all packs (that were not translocated or given foster pups), including those that failed to produce a litter. For example, we wrote that “we also examined how inbreeding might affect components of recruitment [including] the probability of producing a litter,” and “we estimated the probability of producing a litter using logistic regression.” We also provide estimates in Table 3 that show non-significant associations between inbreeding in pups, dams, and sires and the probability of producing a litter (Clement et al. <span>2024</span>).</p><p>We appreciate the interest of Hedrick et al. (<span>2025</span>) in our paper and the larger issue of Mexican wolf management and recovery. Continued management and monitoring of inbreeding, and its relationship to fitness, remain priorities for Mexican wolf recovery. Any decisions about Mexican wolf recovery and management should be guided by the best available science, which currently includes our analysis of inbreeding depression (Clement et al. <span>2024</span>).</p><p>The authors declare no conflicts of interest.</p>","PeriodicalId":17504,"journal":{"name":"Journal of Wildlife Management","volume":"89 3","pages":""},"PeriodicalIF":1.9000,"publicationDate":"2025-02-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/jwmg.70005","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Wildlife Management","FirstCategoryId":"93","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/jwmg.70005","RegionNum":3,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"ECOLOGY","Score":null,"Total":0}
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Abstract

Mexican wolves (Canis lupus baileyi) are a gray wolf subspecies found in northern Mexico and part of the southwestern United States. The subspecies was once extirpated in the wild and the current population is highly inbred, having descended from just 7 founders (U.S. Fish and Wildlife Service [USFWS] 2017). Accordingly, the subspecies is federally listed as endangered, and genetic monitoring and management are key components of the current recovery strategy and downlisting recovery criteria (USFWS 2017). In support of this recovery strategy, we recently evaluated inbreeding depression in wild Mexican wolves in Arizona and New Mexico, USA, from 1998 to 2022 (Clement et al. 2024). Our analysis did not detect any statistical association between inbreeding coefficients in a pack, as estimated from the Mexican wolf pedigree, and the number of pups surviving to 9 months (hereafter, recruitment). Hedrick et al. (2025) provided comments on our work, concluding that Mexican wolves “have shown inbreeding depression” and recommending that Mexican wolves hybridize with northern gray wolves (C. l. occidentalis) to induce genetic rescue. Here, we provide our perspective on inbreeding depression, genetic rescue, and other issues raised by Hedrick et al. (2025).

Hedrick et al. (2025) write rather definitively that Mexican wolves “have shown inbreeding depression.” This statement seems to be based on a combination of a prior expectation that low genetic diversity invariably leads to inbreeding depression and some older studies of Mexican wolves, but the current evidence does not support their claim with regard to recruitment in wild Mexican wolves.

Mexican wolves are descended from 7 founders, so they are highly inbred, which increases the risk of genetic problems. However, many endangered species have experienced genetic bottlenecks, yet some species, including some wolves, have not experienced inbreeding depression (Crnokrak and Roff 1999, Kalinowski et al. 1999, Brzeski et al. 2014, Gooley et al. 2017, Powell et al. 2023) and some have experienced robust post-bottleneck population growth (Harding et al. 2016). Because inbreeding coefficients do not consider the relative occurrence of deleterious alleles in the founders or standing population, inbreeding alone does not establish inbreeding depression. Hedrick et al. (2025) also point to syndactyly as evidence of inbreeding depression; however, they did not support this assertion with any evidence or citations.

While some early studies reported inbreeding depression in Mexican wolves, our recent paper represents the most current and best available science for wild wolves. For example, Fredrickson and Hedrick (2002) reported inbreeding depression in the body sizes of captive wolves, but this is a relatively indirect measure of fitness, compared to our analysis of recruitment in wild wolves. In addition to analyses of captive wolves, Fredrickson et al. (2007) reported inbreeding depression in the maximum number of wild Mexican wolf pups observed during summer. However, our recent analysis benefited from a much larger sample size (352 pack-years vs. 39 pack-years), more timely litter size counts (within 6 weeks vs. within several months), and a more comprehensive fitness metric (combining litter production, litter size, and survival vs. summer pup counts). This is not a criticism of Fredrickson et al. (2007) because they used the best data available at that time, but our recent analysis produced more reliable inferences for recovery actions because of the advantages listed above.

Hedrick et al. (2025) recommend hybridizing with northern gray wolves as a remedy for inbreeding in Mexican wolves. However, hybridization would threaten the integrity of Mexican wolves, bringing clear risks and uncertain benefits, all at a time when the available evidence indicates genetic rescue is not necessary. In recommending hybridization, Hedrick et al. (2025), do not address several important considerations, including the legal status of Mexican wolves as a distinct taxonomic entity (USFWS 2015), the risk of genetic swamping (Edmands 1999, Gippoliti et al. 2018, Odell et al. 2018), and recent progress towards recovery goals (USFWS 2024).

Mexican wolves evolved a distinct genetic and phenotypic profile in Mexico and adjacent portions of the American Southwest, and they fill a unique ecological niche in their native habitats. Accordingly, the USFWS has designated Mexican wolves as a separately listed endangered subspecies (USFWS 2015). Hybridizing with large, Canadian northern gray wolves, as proposed by Hedrick et al. (2025), would compromise the Mexican wolf as a distinct subspecies. Given the smaller body size, higher inbreeding, smaller pack size, and lower abundance of Mexican wolves, hybridization would create a risk of genetic swamping, in which unique portions of the Mexican wolf genome are lost (Odell et al. 2018). Even if hybridization initially induces heterosis, in the long term, introgression of traits that evolved in Canada could lead to outbreeding depression, reducing the fitness of hybridized Mexican wolves in some southwestern habitats (Edmands 1999, Edmands and Timmerman 2003, Gippoliti et al. 2018).

Hedrick et al. (2025) argue that hybridization is necessary because Mexican wolves “have shown inbreeding depression.” As discussed above, their claim rests on older, smaller studies (Fredrickson and Hedrick 2002, Fredrickson et al. 2007), while dismissing a larger and more current study that did not detect inbreeding depression (Clement et al. 2024). Additionally, they do not address the fact that the wild population is currently thriving, which is not consistent with a population in need of genetic rescue. For example, the wild Mexican wolf population has averaged 14% annual growth since 2010, yielding a population that exceeded interim recovery goals by 67% just 5 years into the current recovery plan (USFWS 2024). In addition, gene retention and mean inbreeding in wild Mexican wolves have been better than interim recovery targets (USFWS 2024), indicating that current management is maintaining genetic diversity without hybridization. Hybridization with northern gray wolves given no demonstrable need would be an irreversible ecological experiment that could harm recovery of Mexican wolves.

Hedrick et al. (2025) critiqued our analysis of artificial food caches (which they call “supplemental feeding”). Food caching is a practice in which some denning wolves are provided food during some or all of the pup-rearing season (April to September). Food caches may be provided to wolves near ranches or residential areas to reduce conflicts with people, or to packs with foster pups with the intent of increasing pup survival. Inbreeding levels are not used to decide which packs receive food caches and packs with foster pups were excluded from our analysis. Hedrick et al. (2025) argue for estimating an interaction between inbreeding and food caches on the grounds that food caches may mask inbreeding depression. We fit a simpler additive model (which indicated that food caches increased recruitment) because estimating an interaction for an attenuating effect (i.e., food caches reduce the impact of inbreeding) requires large sample sizes (Sommet et al. 2023). Even without estimating an interaction, we can assess the argument by Hedrick et al. (2025) logically. The overall association between inbreeding and recruitment was not significantly different from zero (Clement et al. 2024). If, as Hedrick et al. (2025) hypothesize, recruitment in unfed packs was negatively associated with inbreeding, then recruitment in fed packs (which constituted 46% of packs) must have a positive association with inbreeding (to maintain the overall slope close to zero). But a positive association between inbreeding and recruitment is biologically implausible and not consistent with a hypothesis of masking. In addition, since 2019 the percentage of packs receiving food has been substantially reduced from that projected in the 2017 Recovery Plan, yet the population has surpassed interim abundance and genetic targets (USFWS 2024). There is no indication that feeding is masking inbreeding depression.

Hedrick et al. (2025) also critiqued our handling of packs that did not produce litters, writing “Clement et al. (2024) only considered inbreeding in litters when there was one or more offspring.” Their statement is incorrect. We estimated the temporal trend in mean inbreeding coefficient only for successful litters (≥1 pup) because non-existent litters are not part of the population. However, our fitness metric, pup recruitment, included all packs (that were not translocated or given foster pups), including those that failed to produce a litter. For example, we wrote that “we also examined how inbreeding might affect components of recruitment [including] the probability of producing a litter,” and “we estimated the probability of producing a litter using logistic regression.” We also provide estimates in Table 3 that show non-significant associations between inbreeding in pups, dams, and sires and the probability of producing a litter (Clement et al. 2024).

We appreciate the interest of Hedrick et al. (2025) in our paper and the larger issue of Mexican wolf management and recovery. Continued management and monitoring of inbreeding, and its relationship to fitness, remain priorities for Mexican wolf recovery. Any decisions about Mexican wolf recovery and management should be guided by the best available science, which currently includes our analysis of inbreeding depression (Clement et al. 2024).

The authors declare no conflicts of interest.

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Hedrick 等人(2025 年)认为杂交是必要的,因为墨西哥狼 "已经表现出近亲繁殖抑制"。如上文所述,他们的说法基于较早的小型研究(Fredrickson 和 Hedrick,2002 年;Fredrickson 等人,2007 年),而否定了一项未发现近亲繁殖抑郁的大型最新研究(Clement 等人,2024 年)。此外,他们也没有考虑到野生种群目前正在蓬勃发展这一事实,而这与需要基因拯救的种群并不相符。例如,自 2010 年以来,墨西哥狼野生种群的年平均增长率为 14%,在当前恢复计划实施 5 年后,其种群数量已超过中期恢复目标 67%(USFWS 2024)。此外,野生墨西哥狼的基因保留率和平均近亲繁殖率均优于中期恢复目标(USFWS 2024),这表明当前的管理在不发生杂交的情况下保持了遗传多样性。Hedrick 等人(2025 年)批评了我们对人工食物贮藏(他们称之为 "补充喂养")的分析。食物储藏是指在幼狼饲养季节(4 月至 9 月)的部分或全部时间,向一些穴居狼提供食物。食物储藏室可能提供给靠近牧场或居民区的狼群,以减少与人类的冲突,或者提供给有寄养幼崽的狼群,以提高幼崽的存活率。近亲繁殖水平并不用于决定哪些狼群会得到食物储藏处,我们的分析也不包括寄养幼狼的狼群。Hedrick 等人(2025 年)认为,近亲繁殖与食物储藏室之间的交互作用可能会掩盖近亲繁殖抑制,因此应估算近亲繁殖与食物储藏室之间的交互作用。我们拟合了一个更简单的加法模型(该模型表明食物贮藏处增加了招募量),因为估计减弱效应(即食物贮藏处减少了近亲繁殖的影响)的交互作用需要较大的样本量(Sommet 等,2023 年)。即使不估计交互作用,我们也可以从逻辑上评估 Hedrick 等人(2025 年)的论点。近亲繁殖与招募之间的总体关联与零无显著差异(Clement 等,2024 年)。如果像 Hedrick 等人(2025 年)假设的那样,未喂养的鼠群的招募与近亲繁殖呈负相关,那么喂养的鼠群(占 46%)的招募与近亲繁殖一定呈正相关(以保持总体斜率接近零)。但近亲繁殖与招募之间的正相关在生物学上是不合理的,也不符合掩蔽假说。此外,自 2019 年以来,与 2017 年恢复计划中的预测相比,接受食物的狼群比例已大幅下降,但该种群已超过中期丰度和遗传目标(USFWS 2024)。没有迹象表明喂食掩盖了近交抑郁。Hedrick 等人(2025 年)还批评了我们对没有产仔的狼群的处理方式,他们写道:"Clement 等人(2024 年)只考虑了有一个或多个后代的狼群的近交情况"。他们的说法是错误的。我们只估算了成功产仔(≥1 只幼仔)的平均近交系数的时间趋势,因为未产仔的幼仔不属于种群的一部分。然而,我们的适应性指标--幼崽招募--包括了所有的幼崽群(没有被转移或给予寄养幼崽),包括那些未能产仔的幼崽群。例如,我们写道:"我们还研究了近亲繁殖可能如何影响招募的组成部分,[包括]产仔概率,"并且 "我们使用逻辑回归估算了产仔概率"。我们还在表 3 中提供了估计值,表明幼狼、母狼和父狼的近亲繁殖与产仔概率之间的关系并不显著(克莱门特等,2024 年)。我们感谢赫德里克等(2025 年)对我们的论文以及墨西哥狼管理和恢复这一更大问题的关注。继续管理和监测近亲繁殖及其与适应性的关系仍然是墨西哥狼恢复的优先事项。有关墨西哥狼恢复和管理的任何决定都应该以现有的最佳科学为指导,其中包括我们对近亲繁殖抑制的分析(Clement 等,2024 年)。
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来源期刊
Journal of Wildlife Management
Journal of Wildlife Management 环境科学-动物学
CiteScore
4.00
自引率
13.00%
发文量
188
审稿时长
9-24 weeks
期刊介绍: The Journal of Wildlife Management publishes manuscripts containing information from original research that contributes to basic wildlife science. Suitable topics include investigations into the biology and ecology of wildlife and their habitats that has direct or indirect implications for wildlife management and conservation. This includes basic information on wildlife habitat use, reproduction, genetics, demographics, viability, predator-prey relationships, space-use, movements, behavior, and physiology; but within the context of contemporary management and conservation issues such that the knowledge may ultimately be useful to wildlife practitioners. Also considered are theoretical and conceptual aspects of wildlife science, including development of new approaches to quantitative analyses, modeling of wildlife populations and habitats, and other topics that are germane to advancing wildlife science. Limited reviews or meta analyses will be considered if they provide a meaningful new synthesis or perspective on an appropriate subject. Direct evaluation of management practices or policies should be sent to the Wildlife Society Bulletin, as should papers reporting new tools or techniques. However, papers that report new tools or techniques, or effects of management practices, within the context of a broader study investigating basic wildlife biology and ecology will be considered by The Journal of Wildlife Management. Book reviews of relevant topics in basic wildlife research and biology.
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Issue Information - Cover Monitoring phenology and behavior of polar bears at den emergence using cameras and satellite telemetry Recovery and genetics of Mexican wolves: a comment on Clement et al. Recovery and genetics of Mexican wolves: a reply to Hedrick et al. Bait trapping of waterfowl increases the environmental contamination of avian influenza virus (AIV)
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