Redefining the Role of Admixture and Genomics in Species Conservation

POLICY PERSPECTIVE Redefining the Role of Admixture and Genomics in Species Conservation Bridgett M. vonHoldt1, Kristin E. Brzeski1, David S. Wilcove1,2, & Linda Y. Rutledge1 1 Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544 2 Woodrow Wilson School of Public and International Affairs, Princeton University, Princeton, NJ 08544 Keywords Abstract Admixture; conservation; endangered species; genomics; hybridization; management; policy. The generation of genome-wide sequence data has brought with it both excit- ing opportunities for conservation and challenges for determining appropriate Correspondence management practices in the face of complex evolutionary histories. Genomic Bridgett M. vonHoldt, 106A Guyot Hall, data can provide deep insight into taxa with complex evolutionary origins, Princeton University, Princeton, NJ 08544, Tel: and is a powerful tool for biologists to obtain a more complete view of an- 609-258-7021, fax: 609-258-7892. cestry. Many policy decisions are encumbered by patterns of gene flow be- E-mail: [email protected] tween species that reveal complex evolutionary histories. Here, we review con- Received servation decisions in admixed species and highlight genomics research that 1 December 2016 demonstrates the commonality of hybridization in wildlife. We encourage a Accepted shift toward a web-of-life framework with emphasis on the need to incorpo- 26 April 2017 rate flexibility in conservation practices by establishing a policy for lineages of admixed ancestry. In particular, we promote a conceptual framework under which hybridization, even extensive hybridization, no longer disqualifies a doi: 10.1111/conl.12371 species from protection; instead, we encourage customized case-by-case management to protect evolutionary potential and maintain processes that sustain ecosystems. Genomics reveal a web-like evolutionary This revelation of frequent gene flow among taxa ne- cessitates a new outlook for conservation. When applied history to conservation, the WOL concept could provide a pro- Traditional taxonomic classification is largely based on ductive framework for biologists and the public to bet- a tree-of-life (TOL) hierarchy and the biological species ter understand the role hybridization plays in speciation concept (BSC), by which descent with modification (Ellstrand et al. 2010; Arnold 2016). If policy favors only in a reproductively isolated lineage leads to speciation the TOL framework, then taxa that experience a high (Dobzhansky 1935). Modern advances in molecular ge- frequency of hybridization with low taxonomic distinc- netic techniques, however, have revealed limitations to tiveness may not receive adequate protection (Rhymer & the BSC, challenging the widespread applicability and Simberloff 1996). In many cases, a WOL framework will validity of using reproductive isolation to define species change the way we prioritize conservation action by fo- (Mallet 1995). Indeed, recent research has demonstrated cusing on adaptive potential through the protection of ge- that evolutionary relationships more closely resemble a nomic and phenotypic diversity, ecological function, and web-of-life (WOL), whereby hybridization is often as im- resilience. Consequently, this will require protection of portant as the TOL evolutionary process of reproductive taxa that have experienced gene flow and introgression isolation (Arnold 2016). Neither model on its own pro- over the course of their evolutionary histories. vides a blanket explanation for all species, with horizontal Advances in genomics now provide opportunities gene transfer through hybridization, introgression, and to collect magnitudes of more genetic data on wild reticulate evolution prevalent in some systems but not populations. Until recently, most assessments regard- others (Arnold & Fogarty 2009). ing taxonomic distinctiveness, “genomic purity,” and Conservation Letters, March/April 2018, 11(2), 1–6 Copyright and Photocopying: C 2017 The Authors. Conservation Letters published by Wiley Periodicals, Inc. 1of6 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. The role of admixture in conservation B. M. vonHoldt et al. hybrid zones were founded on relatively few markers cern (Allendorf et al. 2001); under natural conditions, (microsatellites, mitochondrial DNA, Y chromosome, or combining genomes via hybridization can rapidly con- a few nuclear gene sequences). Important inferences tribute to the generation of novel phenotypic variation have been elucidated with these traditional markers, to facilitate persistence under new selection pressures, but these data have limitations. Evolutionary relation- such as rapidly changing climates (Stebbins 1959; Mallet ships constructed with markers that are predominantly 1995; Becker et al. 2013; Arnold 2016). In an evolution- inherited from one parent as a single non-recombining ary context, hybridization was first defined by Stebbins locus cannot accurately distinguish between species that (1959) as the interbreeding between individuals from dis- originate from true bifurcation events and those that tinct populations with different adaptive norms, which arise from hybridization with subsequent introgression does not exclude cases of secondary contact. Descendants (Seehausen 2004). Although these data can elucidate from a hybridization event carry a mosaic ancestry struc- historical evolutionary lineages and divergence events, ture in their genome, and simply labeling the progeny they are generally ineffective for delineating species as “hybrids” can be misleading. For example, in a pro- where introgressive hybridization and/or incomplete lin- cess sometimes referred to as “mitochondrial capture,” eage sorting are evident. Genomic sequencing, however, animals with introgressed mtDNA are considered hybrids wields more power to differentiate between hybridiza- even though backcrossing has effectively eliminated any tion and incomplete lineage sorting, improve analytical nuclear signature of the introgressed species (Good et al. precision to estimate population parameters, and provide 2008; Keller et al. 2010). Similarly, organisms that have detailed information on adaptive and functional loci, ancient or recent hybrid origins but have become ge- although there are several practical limitations to con- netically distinct are sometimes still considered hybrids sider (Harrison et al. 2014). For example, whole genome (Burrell et al. 2009; Larsen et al. 2010). Again, variabil- analysis of polar bears and brown bears identified di- ity in systems is evidenced in the observation by Stebbins rectional gene flow that was not a threat to polar bear (1959) that the evolutionary role of hybridization is much persistence; however, divergence time estimates varied greater in some lineages than in others. (e.g., 343,000-479,000 vs. 4-5 million years ago, detailed Many taxa with admixed genomes, particularly mam- in Cahill et al. 2015), suggesting cautious assessment and mals, face a challenging stigma that is bound to their validation are required to reach consensus. history of hybridization. Excluding contemporary cases Conservation genomics is becoming accessible for a di- where anthropogenic-mediated hybridization results in versity of taxa and promises new opportunities for ap- sterile or maladaptive hybrids (Todesco et al. 2016), the plied wildlife research (Allendorf et al. 2010; Ellegren & view that hybridization “eliminates” species through ho- Galtier 2016; Garner et al. 2016). Genomic studies are mogenization (Mayr 1963) is being re-envisioned since necessary for providing evidence of the WOL framework, hybrids can oftentimes be fertile, genetically isolated from where admixture is recognized as part of the specia- parental forms, and represent viable adaptive evolution tion process. Consequently, the WOL framework estab- (Mallet 1995; Arnold 2016; Hamilton & Miller 2016; lishes an inclusive foundation for the conservation of Table S1). For example, ancient admixture with subse- taxa because reproductive isolation is not a prerequisite quent introgression of functional variation in Lake Vic- for taxonomic classification. Though the complexity of toria cichlids allowed multiple adaptive radiation events the WOL model is a drawback, it provides a more accu- originating from a hybrid swarm (Meier et al. 2017). rate representation of evolutionary processes. This model As such, hybrid zones can be driven by environmen- is, therefore, important for recovery strategies that aim tal gradients where hybridization provides a platform on to increase genetic diversity and ecological adaptation of which selection can act by way of stable hybrid forms small, imperiled populations (Ellstrand et al. 2010; Jackiw that contribute to distinct evolutionary change (Steb- et al. 2015; Arnold 2016). bins 1959; Becker et al. 2013). The natural emergence of these nascent genomes can be evolutionarily successful because they have a new capacity to respond to chang- The evolutionary context of ing conditions and new environments. However, admix- hybridization and admixed genomes ture can present a problem for conservation when oc- curring in species at risk of extinction, particularly when Major shifts in evolutionary space, such as intraspecific anthropogenic events are to blame. Historically, conser- adaptations or species radiations, often require novel vation efforts have ignored

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