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Conservation in the Era of Molecular Phylogenetics

Molecular tools have given systematists new ways to resolve phylogenies and population networks and thus new ways to delimit species and other units of conservation concern. Genetics has created new ways of thinking about what a species is, and this has led to healthy debates about species delimitation. In some countries such as Germany, conservation legislation takes into account the genetics of organisms as well as their species limits. The Nationale Strategie zur Biologischen Vielfalt (National Strategy for Biological Diversity of Germany, BMU 2007) recognizes that the entire gene pool of a species must be protected. While this may not always be possible, the reason for this approach is based on the desire to protect distinct lineages.

Populations are often locally adapted and may be on different evolutionary trajectories even within what is recognized as a single species. The term Evolutionary Significant Unit or ESUs was originally coined to reflect the importance of these units in conservation decisions (Ryder 1986; Moritz 1994). ESUs may be at the species level or below and ESU definitions generally include the idea that the ESU is currently geographically isolated from other ESUs, that there is genetic differentiation at neutral markers, or that there is local phenotypic variation. The term ESU has since changed to reflect both evolutionary processes along with ecological exchangeability. The crosshair analysis advocated by Crandall et al. (2000) uses tests of null hypotheses in four categories (genetic, ecological, recent, and history) to determine whether populations should be considered ESUs or not. Species are not static, but evolving; if given enough time, ESUs may evolve into entities that require a different taxonomic status, e.g., a population may become a new species. ESUs may represent unique gene pools and may be of special conservation concern; proper conservation action can be taken only if they are recognized.

Molecular genetics has also allowed researchers to identify cryptic species, species that are morphologically indistinguishable (or nearly so) but exhibit significant genetic divisions that form species boundaries (Pfenninger and Schwenk 2007). These discoveries have helped systematists further understand the mechanisms that drive the speciation process, such as sympatric reproductive isolation without morphological differentiation, but they also have conservation implications (Bickford et al. 2007). Cryptic species represent a previously unrecognized part of the biota of a region and thus may be important to conservation biologists who are interested in identifying and understanding biodiversity hotspots. In bats, many previously unrecognized cryptic species are now being found through molecular assays even in very well-studied areas (Mayer et al. 2007). Early results from bar coding work in Southeast Asia suggest that the number of bat species may be twice that currently recognized (Francis et al. 2010). The level of discovery of new taxa in the last decade has generally corroborated this estimate (Table 16.1).

A classic example of a cryptic species hiding in plain sight is the European pipistrelle (Pipistrellus pipistrellus). One of the most common bats throughout its range, the European pipistrelle was not recognized as a cryptic complex until echolocation data suggested the presence of more than one species of pipistrelle occurring in sympatry throughout much of Europe (Jones and van Parijs 1993; Barlow 1997; Barlow and Jones 1997). Since the early echolocation studies, mitochondrial data (Hulva et al. 2004), microsatellite data (Hulva et al. 2010), information on foraging (Davidson-Watts and Jones 2005), and habitat selection data (Davidson-Watts et al. 2006) have further corroborated the split of the European pipistrelle into two distinct species (P. pipistrellus and Pipistrellus pygmaeus). Similar echolocation studies in Southeast Asia of hipposiderid bats (Kingston et al. 2001; Thabah et al. 2006) and African Rhinolophus (Taylor et al. 2012) have shown that these groups likely contain many cryptic species that can be distinguished by distinct phonic profiles, but not so easily by morphology. In many cases, molecular work remains to be conducted to clarify the numbers and limits of species in these complexes.

Molecular tools can now be used to characterize biodiversity in a more efficient manner than could be done in the past, particularly in poorly studied regions of the world. However, these tools must be used with caution, as not every new mitochondrial clade warrants recognition as a distinct species—some genes are known to be hypervariable and poor indicators of species limits (Engstrom et al. 2004; Lohse 2009; Galtier et al. 2009). The phylogenetic signal for hybridizing species may look very similar to incomplete lineage sorting (e.g., both phenomena would result in non-monophyletic trees) and therefore requires more genetic data and stricter quantitative assessments of genetic data to test different evolutionary scenarios (Maddison 1997; Yu et al. 2012). Many molecular studies of bats published in recent years have failed to review important elements such as the morphology or echolocation call structure of putative species, or have failed to include a sufficient number of genes or individuals. Mitochondrial clades may point to the need for more research into a potential species complex, but such clades cannot be readily assumed to represent a new species. The recent discovery of multiple allopatric mitochondrial lineages of Pteronotus parnellii (Clare et al. 2011) Chrotopterus auritus, Glossophaga soricina, and Saccopteryx bilineata (Clare 2011) indicates that deep divergences may exist within these species, but further study of genetic, morphological, or behavioral characters is needed as noted by these authors. Even in well-studied regions, such as Europe, cryptic species may have only been recently recognized as new phylogenetic methods and more nuclear data have become available, such as the Natterer's bat (Myotis nattereri) complex (Salicini et al. 2011). Mitochondrial divergence may also reflect sex-based differences in dispersal rather than new species. For example, Ozark big-eared bats (Corynorhinus townsendii ingens) have low levels of mitochondrial divergence between caves, but their microsatellite data indicate that there is likely male-mediated gene flow between populations (Weyandt et al. 2005).

Examples exist of cases where mitochondrial data have been misleading in bats. A cautionary tale is that of two subspecies of Myotis lucifugus (M. lucifugus and M. carissima), which exhibited enough mitochondrial divergence that they could have been recognized as separate species on the basis of molecular evidence alone (Dewey 2006). However, analyses of ten additional nuclear markers have shown that both these subspecies are experiencing high levels of gene flow, resulting in the absence of population structure even if these were historically separate populations. Additionally, no morphological characters diagnose the mitochondrial clades (Lausen et al. 2008). Consequently, there is no justification, despite the mitochondrial indicators, for recognizing these subspecies as separate species.

In contrast, Goodman et al. (2009) used a combined molecular and morphological dataset to resolve cryptic species in Miniopterus manavi. This study demonstrates a “best practices” approach to resolving widespread species complexes. Previous research using only mitochondrial data suggested that M. manavi in Madagascar and the Comoros represented unique lineages. However, sampling was limited and the relationships between clades were not fully resolved (Weyeneth et al. 2008). Using increased geographic sampling and morphological comparisons of type specimens, each of the clades was more clearly defined. Miniopterus aelleni was recognized as a new species, and its species diagnosis and description was accompanied by photographs of a live individual and skulls, and illustrations of dental characters (Goodman et al. 2009). Despite the relative rarity of M. aelleni to M. manavi on Madagascar, both species were found in several protected areas and the authors did not suggest further conservation action.

Extensive sampling throughout the geographic range of the relevant species is needed when attempting to resolve the relationships within a species complex. Simulation data suggests that more complete taxonomic sampling improves phylogenetic accuracy (Pollock et al. 2002). Too much missing data, either in the form of missing characters (e.g., missing genetic loci or using only mitochondrial data for some taxa) or missing taxa (e.g., incomplete geographic sampling) can lead to unresolved trees or incorrect inferences through phenomena such as long-branch attraction (Wiens 2003, 2006).

Currently, the field of molecular phylogenetics is undergoing a major shift away from locus-by-locus data collection to next-generation sequencing methods (also called high-throughput sequencing) that will allow for the collection of massive datasets in a relatively short period of time (Faircloth et al. 2012; Lemmon et al. 2012; Lemmon and Lemmon 2012). As prices fall and computational pipelines are developed to deal with the influx of data, taxonomically complex problems may be resolved by the increased availability of molecular character data. Genomic advances will also allow for detection of signs of natural selection in recent history (e.g., Pickrell et al. 2009 in humans; vonHoldt et al. 2010 in dogs), which could be used to determine how recent historical events such as climate change or human disturbance have affected natural populations. Having more data may not be the only solution to taxonomic problems, however—more powerful computational models means greater ability to analyze multilocus datasets that are already available. By taking cues from population genetics and phylogeography, historical models can now be incorporated into analyses to understand the effects of microevolutionary processes on species histories (Edwards and Beerli 2000). Establishing that a tip on a phylogenetic tree is truly representative of a species, and not just a genetic lineage, is fundamental to the goals of systematics and necessary prior to further analyses about speciation and diversification (Edwards 2009).

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