Craig Moritz

Defining 'Evolutionarily Significant Units' for conservation.

writing in the first issue of TREE, Ryder’ brought the term ‘Evolutionarily Significant Unit’ (ESU) to the attention of a broad audience of ecologists and evolutionary biologists. The ESU concept was developed to provide a rational basis for prioritizing taxa for conservation effort (e.g. captive breeding), given that resources are limited and that existing taxonomy may not adequately reflect underlying genetic diversity*. With the explicit recognition of the genetic component of biodiversity in conservation legislation of many countries and in the Convention on Biological Diversity, the ESU concept is set to become increasingly significant for conservation of natural as well as captive populations.

Evolution of Animal Mitochondrial DNA: Relevance for Population Biology and Systematics

In the past decade, mitochondrial DNA (mtDNA) analysis has become established as a powerful tool for evolutionary studies of animals. These studies, recently reviewed by Avise (8) and Wilson et al (149), have used mtDNA analyses to provide insights into population structure and gene flow, hybridization, biogeography, and phylogenetic relationships. Major advances have been made in our understanding of the molecular biology of animal mtDNA (reviewed in 7, 28). A powerful synergism exists between the two fields of research: Evolutionary studies provide comparative data on mtDNA organization and function, and molecular investigations can, and should, improve the level of sophistication of evolutionary studies that use mtDNA. Here we focus on molecular aspects of animal mtDNA that are especially relevant to its use in evolutionary studies. Thus, we consider the form and frequency of three types of change in mtDNA: base substitution, length variation, and sequence rearrangement. Attention is also given to the nature and possible consequences of interactions between nuclear and mitochondrial (mt) genes. In the concluding sections, we discuss the way in which the knowledge of molecular processes allows informed use of mtDNA variation in evolutionary studies. Only animal mtDNAs are considered. The molecular biology and evolution of chloroplast DNA and nonmetazoan mtDNAs have been reviewed elsewhere (41, 66, 111, 121, 123).

Strategies to Protect Biological Diversity and the Evolutionary Processes That Sustain It

Conservation planning has tended to focus more on pattern (representation) than process (persistence) and, for the former, has emphasized species and ecosystem or community diversity over genetic diversity. Here I consider how best to incorporate knowledge of evolutionary processes and the distribution of genetic diversity into conservation planning and priority setting for populations within species and for biogeographic areas within regions. Separation of genetic diversity into two dimensions, one concerned with adaptive variation and the other with neutral divergence caused by isolation, highlights different evolutionary processes and suggests alternative strategies for conservation. Planning for both species and areas should emphasize protection of historically isolated lineages (Evolutionarily Significant Units) because these cannot be recovered. By contrast, adaptive features may best be protected by maintaining the context for selection, heterogeneous landscapes, and viable populations, rather than protecting specific phenotypes. A useful strategy may be to (1) identify areas that are important to represent species and (vicariant) genetic diversity and (2) maximize within these areas the protection of contiguous environmental gradients across which selection and migration can interact to maintain population viability and (adaptive) genetic diversity. These concepts are illustrated with recent results from analysis of a rainforest fauna from northeast Australia.

DNA Barcoding: Promise and Pitfalls

In this issue of PLoS Biology, Hebert et al. (2004) have set out to test the resolution and performance of “DNA barcoding,” using a single mtDNA gene, cytochrome c oxidase I (COI), for a sample of North American birds. Before turning to details of this study, it is useful as context to consider the following questions: What is DNA barcoding, and what does it promise? What is new about it? Why is it controversial? What are the potential pitfalls?

Applications of mitochondrial DNA analysis in conservation: a critical review

Patterns of variation in mitochondrial DNA (mtDNA) increasingly are being investigated in threatened or managed species, but not always with clearly defined goals for conservation. In this review I identify uses of mtDNA analysis which fall into two different areas: (i) ‘gene conservation’ ‐ the identification and management of genetic diversity, and (ii) ‘molecular ecology’ ‐ the use of mtDNA variation to guide and assist demographic studies of populations. These two classes of application have different conceptual bases, conservation goals and time‐frames. Gene conservation makes extensive use of phylogenetic information and is, in general, most relevant to long‐term planning. Appropriate uses here include identification of Evolutionarily Significant Units and assessment of conservation priority of taxa or areas from an evolutionary perspective. Less appropriate are inferences about fitness from within‐population diversity and about species boundaries. Molecular ecology makes more use of allele frequencies and provides information useful for short‐term management of populations. Powerful applications are to identify Management Units and to define and use naturally occurring genetic tags. Estimating demographic parameters, e.g migration rate and population size, from patterns of mtDNA diversity is fraught with difficulty, particularly where populations are fluctuating, and is unlikely to produce quantitative estimates sufficiently accurate to be useful for practical management of contemporary populations. However, through comparative studies, mtDNA analysis can provide qualitative signals of population changes, allowing efficient targeting of resource‐intensive ecological studies. Thus, there are some relatively straightforward uses of mtDNA, preferably in conjunction with assays of nuclear variation, that can make a significant contribution to the long‐term planning and short‐term execution of species recovery plans.

Stability Predicts Genetic Diversity in the Brazilian Atlantic Forest Hotspot

Biodiversity hotspots, representing regions with high species endemism and conservation threat, have been mapped globally. Yet, biodiversity distribution data from within hotspots are too sparse for effective conservation in the face of rapid environmental change. Using frogs as indicators, ecological niche models under paleoclimates, and simultaneous Bayesian analyses of multispecies molecular data, we compare alternative hypotheses of assemblage-scale response to late Quaternary climate change. This reveals a hotspot within the Brazilian Atlantic forest hotspot. We show that the southern Atlantic forest was climatically unstable relative to the central region, which served as a large climatic refugium for neotropical species in the late Pleistocene. This sets new priorities for conservation in Brazil and establishes a validated approach to biodiversity prediction in other understudied, species-rich regions.

INTEGRATING PHYLOGENETICS AND ENVIRONMENTAL NICHE MODELS TO EXPLORE SPECIATION MECHANISMS IN DENDROBATID FROGS

Abstract We developed an approach that combines distribution data, environmental geographic information system layers, environmental niche models, and phylogenetic information to investigate speciation processes. We used Ecuadorian frogs of the family Dendrobatidae to illustrate our methodology. For dendrobatids there are several cases for which there is significant environmental divergence for allopatric and parapatric lineages. The consistent pattern that many related taxa or nodes exist in distinct environmental space reinforces Lynch and Duellmans hypothesis that differential selection likely played an important role in species differentiation of frogs in the Andes. There is also some evidence that the Río Esmeraldas basin is a geographic barrier to species distributed in low to middle elevations on the western side of the Andes. Another useful aspect of this approach is that it can point to common environmental parameters that correlate with speciation. For dendrobatids, sister clades generally segregate along temperature/elevational and/or seasonality axes. The joint analysis of environmental and geographic data for this group of dendrobatid frogs has identified potentially important speciation mechanisms and specific sister lineages that warrant intensive study to test hypotheses generated in this investigation. Further, the method outlined in this paper will be increasingly useful as knowledge of distribution and phylogeny of tropical species increases.

Coalescent-based species delimitation in an integrative taxonomy

The statistical rigor of species delimitation has increased dramatically over the past decade. Coalescent theory provides powerful models for population genetic inference, and is now increasingly important in phylogenetics and speciation research. By applying probabilistic models, coalescent-based species delimitation provides clear and objective testing of alternative hypotheses of evolutionary independence. As acquisition of multilocus data becomes increasingly automated, coalescent-based species delimitation will improve the discovery, resolution, consistency, and stability of the taxonomy of species. Along with other tools and data types, coalescent-based species delimitation will play an important role in an integrative taxonomy that emphasizes the identification of species limits and the processes that have promoted lineage diversification.

Comparative phylogeography: concepts and applications

This special issue of Molecular Ecology celebrates the birth of phylogeography 10 years ago (Avise et al. 1987). Because the discipline has deep roots in historical biogeography and population genetics, phylogeography was heralded as a bridge linking the study of microand macroevolutionary processes. The initial and still dominant infrastructure for this bridge has been mitochondrial DNA (mtDNA) analyses which have permitted genealogical traces to be followed across the genetic boundaries between populations, species and higher taxonomic levels. In his personal reflection, Avise (1998) documents the explosive growth of phylogeography in the decade since its inception and notes many of the hallmark studies that have provided the empirical and conceptual link between systematics and population genetics. Celebrations are often times of renewal, and thus this special issue of Molecular Ecology aims not only to review the past but also to present a blend of theoretical and empirical papers with the hope of invigorating the field. Phylogeography and its predominant reliance on (animal) mtDNA has led to a body of descriptive data that are impressive in terms of their sheer comparative scope. For example, comparisons of mtDNA divergence between sister taxa of North American birds (Bermingham et al. 1992; Klicka & Zink 1997), South American rodents and marsupials (da Silva & Patton 1998) and frogs and reptiles across the Australian Wet Tropics (Schneider et al. 1998) have significantly discounted Late Pleistocene models of speciation and suggested that many species pairs are older than previously appreciated. Several articles in this issue presage the potential of comparative phylogeographic analyses and demonstrate that the shift from RFLP-based assays to direct determination of DNA nucleotide sequence has permitted increasingly fruitful cross-taxa comparisons of evolutionary history. In turn, we project that comparative phylogeographic analysis will permit detailed studies of landscape evolution, including the dispersal of taxa through a region, speciation, adaptive radiation, and extinction; in other words, investigation of the fundamental links between population processes and regional patterns of diversity and biogeography. The (typically) slower evolutionary rate of chloroplast DNA (Schaal et al. 1998) has limited the contribution of plants to phylogeography and our nascent knowledge of landscape evolution. We anticipate that plant phylogeography will increase in importance, thus refining our interpretation of historical landscape assembly and maintenance, as our understanding of the mutational basis of microsatellite evolution improves and permits this class of molecular markers to be used in comparative context. Certainly one clear empirical success of mtDNA-based phylogeography has been the improved description of the geographical distribution, phylogenetic relationships and genetic distances among evolutionary lineages of animals, leading, in turn, to a better understanding of regional biogeography and areas of endemism. Articles presented in this issue summarize and discuss the evolutionary landscapes of North America (Bernatchez & Wilson 1998), lower Central America (Bermingham & Martin 1998), Amazonia (da Silva & Patton 1998), Europe (Taberlet et al. 1998), the Australian Wet Tropics (Schneider et al. 1998) and Hawaii (Roderick & Gillespie 1998; see also Fleischer et al. 1998). These studies demonstrate the importance of combining molecular phylogeographic evidence with independent information on landscape history obtained from geology, palaeopalynology, etc. Of course there is a long way to go. One of the many challenges lying ahead is the comparative phylogeographic description of marine species, owing in part to the vast and disjunct geographical scale of many marine populations (Shulman & Bermingham 1995; Palumbi 1997). Meeting this challenge will undoubtedly provide contrasts and insights as sharp as those emerging from comparisons of temperate and tropical terrestrial evolutionary landscapes. Comparative phylogeographic analyses can contribute to broader studies of ecology and evolution in a number of ways. First, phylogeographic analysis can identify historically and evolutionarily independent regions that can be considered as natural replicates amongst which generalizations about specific processes can be tested statistically. For example, the evolutionary response to selection gradients can be compared across Molecular Ecology (1998) 7, 367–369

Reinforcement drives rapid allopatric speciation

Allopatric speciation results from geographic isolation between populations. In the absence of gene flow, reproductive isolation arises gradually and incidentally as a result of mutation, genetic drift and the indirect effects of natural selection driving local adaptation. In contrast, speciation by reinforcement is driven directly by natural selection against maladaptive hybridization. This gives individuals that choose the traits of their own lineage greater fitness, potentially leading to rapid speciation between the lineages. Reinforcing natural selection on a population of one of the lineages in a mosaic contact zone could also result in divergence of the population from the allopatric range of its own lineage outside the zone. Here we test this with molecular data, experimental crosses, field measurements and mate choice experiments in a mosaic contact zone between two lineages of a rainforest frog. We show that reinforcing natural selection has resulted in significant premating isolation of a population in the contact zone not only from the other lineage but also, incidentally, from the closely related main range of its own lineage. Thus we show the potential for reinforcement to drive rapid allopatric speciation.