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Prioritization of taxa for conservation must rest on a foundation of correctly identified species boundaries, enhanced by an understanding of evolutionary history and phylogenetic relationships. Therefore, we can incorporate both evolutionary and ecological processes into efforts to sustain biodiversity. In this issue of Molecular Ecology, Malaney & Cook (2013) highlight the critical value of an evolutionary biogeographical approach, combining multilocus phylogeography with climatic niche modelling to infer phylogenetically weighted conservation priorities for evolutionary lineages of jumping mice across North America. Remarkably, they find that the Preble's meadow jumping mouse (Zapus hudsonius preblei), long debated as a threatened taxon, in fact represents the southern terminus of a relatively uniform lineage that expanded well into Alaska during the Holocene. By contrast, some other relictual and phylogenetically divergent taxa of jumping mice likely warrant greater conservation priority. This study highlights the value of integrative approaches that place current taxonomy in a broader evolutionary context to identify taxa for conservation assessment, but also highlights the challenges in maintaining potential for adaptive responses to environmental change.
It should be obvious that sound taxonomy, including correct delimitation of taxa and understanding of their evolutionary history, should underpin prioritization of taxa for conservation effort. A related, more challenging goal is to identify key evolutionary processes and strategies to maintain these. In this context, it is useful to separate processes along two axes of concern—historical and adaptive (Moritz 2002). The historical axis focuses on identifying and protecting major, independently evolving lineages, whether or not these are recognized in current taxonomy, and can be extended to consider how much unique evolutionary history is represented by the lineage in question (Isaac et al. 2007). For this purpose, multilocus molecular analyses, including recently developed, coalescent-based methods for delimiting lineages and estimating species trees (Fujita et al. 2012; Carstens et al. 2013) are powerful. The adaptive axis, which seeks to maintain capacity for evolutionary response, is much more challenging from a purely molecular perspective and typically rests on assessments of morphologic diversity or ecological niches (Crandall et al. 2000).
Jumping mice (Zapus, Fig. 1) are a widespread clade in North America with numerous described species, subspecies and, now revealed, evolutionary lineages that sometimes are discordant with subspecies. Multilocus (mtDNA and four nDNA genes) analyses of the entire clade reveal some surprises—most notably that Z. h. preblei is not distinct, but rather is embedded within a widespread lineage that has expanded into high latitudes following post-last glacial maximum (LGM) retraction of the glacial ice sheets. The key result, derived from a combination of multilocus phylogenetic analyses, tests for population expansion and spatial modelling under LGM and current climates, is convincing. Clearly, the next step is to apply emerging methods for molecular species delimitation (Fujita et al. 2012; Carstens et al. 2013). Several previous studies compared Z. h. preblei with just the geographically adjacent subspecies and found the former to be distinct—a result confirmed here. It was only through sampling across a broader geographical and taxonomic scale of previously unrepresented northern subspecies that the true nature of Z. h. preblei was revealed. There is a message here for all of us.
Figure 1. Jumping mouse from the southwestern lineage (Malaney & Cook 2013, Zapus hudsonius luteus) from the America Southwest (New Mexico and Arizona) proposed endangered under USFWS. Photograph kindly provided by Greg Wright.
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In relation to the adaptive component of diversity, Malaney & Cook (2013) assessed ‘ecological exchangeability’ through climatic niche analysis, finding no difference between Z. h. preblei and other populations of the northern lineage of Z. hudsonius of which it is part. This, of course, is but one dimension of the ecological niche, yet the analysis serves to highlight that Z. h. preblei does not inhabit unique climatic space within its taxon. Additional insights might well come from detailed comparative analyses of morphology (e.g. ecologically relevant skull characters). As Malaney & Cook (2013) note, this now needs to be done for Z. h. preblei in the context of other populations from its widespread lineage. These and other authors (see Phillimore & Owens 2006) are quick to portray subspecies as ‘antiquated intraspecific taxonomy’ when these taxa are not also divergent at neutral loci. Subspecies as originally construed (e.g. Mayr 1942) were taken to reflect nonoverlapping geographical subdivisions in phenotype. Where geographical variation is clinal, Mayr (1963) recommended that subspecies not be recognized. There is debate surrounding the use of subspecies which we will not enter into here, other than to highlight what Haig et al. (2006) pointed out, ‘infraspecific diversity is important to protect in conservation as it represents evolutionary potential’ and should be incorporated in setting conservation priorities. Phenotypic variation without indication of associated genetic variation has provided evidence of local adaptation to different ecological conditions (see Davis et al. 2008; Cicero & Koo 2012). On this note, it is also worth considering what sort of evidence might be obtained to test whether populations of Z. h. preblei, located at the southern limit of the lineage distribution, retain unique adaptations in the context of ongoing climate change (Hampe & Petit 2005; Hampe & Jump 2011).
To assess relative conservation priorities, Malaney & Cook (2013) employed the EDGE protocol (Isaac et al. 2007), which integrates phylogenetic distinctiveness with population trend data as more commonly applied for IUCN red listing. Given the new phylogenetic results, it is no surprise that they find Z. h. preblei to rank low relative to other lineages of jumping mice, especially the Uinta jumping mouse (Z. p. utahensis), which though declining is not yet listed. A novel and intriguing aspect of their analysis was to incorporate inferred population dynamics post-LGM, as well as recent population trends. Although the actual weights for prioritization of the taxa are not given, Malaney & Cook (2013) apply a method that assesses historical and contemporary population size and range to score priorities. They contrast a recent history of population and range expansion in the northern lineage containing Z. h. preblei, with, for example, signatures of population reduction in the relictual Uinta mouse. This raises the question of whether, and how, historical demography should be incorporated within conservation assessments. Should we be more concerned where recent (anthropogenic) population declines reflect long-term (natural?) range contraction, or where recent declines oppose a hypothesized long-term pattern of expansion? An important outcome of Malaney & Cook (2013) was the proposed endangered status for Z. h. luteus (Fig. 1), which highlights the utility of applying an evolutionary biogeographical approach in understanding anthropogenic declines.
In the context of ongoing habitat loss, invasive species and now climate change, the pressure to prioritize taxa for conservation investment will only grow. Malaney & Cook (2013) make a valuable point about the utility of museums as resources to assess historical evolutionary processes and shifts in ecological and evolutionary patterns. The concepts and tools to rigorously assess the evolutionary independence and distinctiveness of candidate taxa are in hand and should be deployed routinely. By contrast, we are far from defining a consistent approach to quantifying the ‘adaptive axis’ of diversity, as is crucial to maintain capacity for evolutionary response to the multidimensional and rapid environmental challenges faced by species. Perhaps for now the simplest approach is best—maintain viable (meta) populations across the full ecological breadth of a given species. As evolution within species occurs across both historical and adaptive axes (e.g. evolutionarily significant units, subspecies), we need to incorporate both in conservation planning. Consideration therefore should be given to extending IUCN red list criteria to include changes in environmental space occupied by species, such as that shown by Malaney & Cook (2013).