Alexandra Pavlova

Using genomics to characterize evolutionary potential for conservation of wild populations

Genomics promises exciting advances towards the important conservation goal of maximizing evolutionary potential, notwithstanding associated challenges. Here, we explore some of the complexity of adaptation genetics and discuss the strengths and limitations of genomics as a tool for characterizing evolutionary potential in the context of conservation management. Many traits are polygenic and can be strongly influenced by minor differences in regulatory networks and by epigenetic variation not visible in DNA sequence. Much of this critical complexity is difficult to detect using methods commonly used to identify adaptive variation, and this needs appropriate consideration when planning genomic screens, and when basing management decisions on genomic data. When the genomic basis of adaptation and future threats are well understood, it may be appropriate to focus management on particular adaptive traits. For more typical conservations scenarios, we argue that screening genome‐wide variation should be a sensible approach that may provide a generalized measure of evolutionary potential that accounts for the contributions of small‐effect loci and cryptic variation and is robust to uncertainty about future change and required adaptive response(s). The best conservation outcomes should be achieved when genomic estimates of evolutionary potential are used within an adaptive management framework.

Evolutionary refugia and ecological refuges: key concepts for conserving Australian arid zone freshwater biodiversity under climate change.

Refugia have been suggested as priority sites for conservation under climate change because of their ability to facilitate survival of biota under adverse conditions. Here, we review the likely role of refugial habitats in conserving freshwater biota in arid Australian aquatic systems where the major long-term climatic influence has been aridification. We introduce a conceptual model that characterizes evolutionary refugia and ecological refuges based on our review of the attributes of aquatic habitats and freshwater taxa (fishes and aquatic invertebrates) in arid Australia. We also identify methods of recognizing likely future refugia and approaches to assessing the vulnerability of arid-adapted freshwater biota to a warming and drying climate. Evolutionary refugia in arid areas are characterized as permanent, groundwater-dependent habitats (subterranean aquifers and springs) supporting vicariant relicts and short-range endemics. Ecological refuges can vary across space and time, depending on the dispersal abilities of aquatic taxa and the geographical proximity and hydrological connectivity of aquatic habitats. The most important are the perennial waterbodies (both groundwater and surface water fed) that support obligate aquatic organisms. These species will persist where suitable habitats are available and dispersal pathways are maintained. For very mobile species (invertebrates with an aerial dispersal phase) evolutionary refugia may also act as ecological refuges. Evolutionary refugia are likely future refugia because their water source (groundwater) is decoupled from local precipitation. However, their biota is extremely vulnerable to changes in local conditions because population extinction risks cannot be abated by the dispersal of individuals from other sites. Conservation planning must incorporate a high level of protection for aquifers that support refugial sites. Ecological refuges are vulnerable to changes in regional climate because they have little thermal or hydrological buffering. Accordingly, conservation planning must focus on maintaining meta-population processes, especially through dynamic connectivity between aquatic habitats at a landscape scale.

A tale of two flatties : different responses of two terrestrial flatworms to past environmental climatic fluctuations at Tallaganda in montane southeastern Australia.

Comparative phylogeographic studies of animals with low mobility and/or high habitat specificity remain rare, yet such organisms may hold fine‐grained palaeoecological signal. Comparisons of multiple, codistributed species can elucidate major historical events. As part of a multitaxon programme, mitochondrial cytochrome oxidase I (COI) variation was analysed in two species of terrestrial flatworm, Artioposthia lucasi and Caenoplana coerulea. We applied coalescent demographic estimators and nested clade analysis to examine responses to past, landscape‐scale, cooling‐drying events in a model system of montane forest (Tallaganda). Correspondence of haplotype groups in both species to previously proposed microbiogeographic regions indicates at least four refuges from cool, dry conditions. The region predicted to hold the highest quality refuges (the Eastern Slopes Region), is indicated to have been a long‐term refuge in both species, but so are several other regions. Coalescent analyses suggest that populations of A. lucasi are declining, while C. coerulea is expanding, although stronger population substructure in the former could yield similar patterns in the data. The differences in spatial and temporal genetic variation in the two species could be explained by differences in ecological attributes: A. lucasi is predicted to have lower dispersal ability but may be better able to withstand cold conditions. Thus, different contemporary population dynamics may reflect different responses to recent (Holocene) climate warming. The two species show highly congruent patterns of catchment‐based local genetic endemism with one another and with previously studied slime‐mould grazing Collembola.

PHYLOGEOGRAPHIC PATTERNS IN MOTACILLA FLAVA AND MOTACILLA CITREOLA: SPECIES LIMITS AND POPULATION HISTORY

Abstract We conducted phylogeographic analyses of Motacilla flava (Yellow Wagtail) and M. citreola (Citrine Wagtail). We analyzed mitochondrial DNA sequences from 167 M. flava specimens obtained from 17 localities throughout Eurasia and Alaska, and 38 specimens of M. citreola obtained from 7 Eurasian localities. Phylogenetic analysis revealed three clades within traditionally recognized M. flava: Europe and southwestern Asia, northeastern Eurasia, and southeastern Asia. Those groups should be considered species, because together they are not monophyletic, and are interspersed with M. citreola, M. cinerea, and M. alba. Motacilla citreola also is paraphyletic, consisting of two species-level groups. Northeastern and southeastern groups of M. flava each appear to be sister taxa to eastern and western groups of M. citreola, respectively. Together those four groups form a clade, whereas the western M. flava group is considerably more distant. Within each of the three groups of M. flava, and the two groups of M. citreola, little phylogeographic structure was detected. Signatures of past population expansion are evident for some populations of M. flava; expansion is more recent in Moscow, Kursk (western group), Yamal, and Anabar (northeastern group), and older in Tyva and Vyatka (western group). A history of population stability is inferred for the Yamal population of M. citreola. Nested-clade analyses detected contiguous range expansion for southeastern M. flava and restricted gene flow with isolation by distance for northeastern M. flava and eastern M. citreola.

Perched at the mito-nuclear crossroads: divergent mitochondrial lineages correlate with environment in the face of ongoing nuclear gene flow in an Australian bird.

Relationships among multilocus genetic variation, geography, and environment can reveal how evolutionary processes affect genomes. We examined the evolution of an Australian bird, the eastern yellow robin Eopsaltria australis, using mitochondrial (mtDNA) and nuclear (nDNA) genetic markers, and bioclimatic variables. In southeastern Australia, two divergent mtDNA lineages occur east and west of the Great Dividing Range, perpendicular to latitudinal nDNA structure. We evaluated alternative scenarios to explain this striking discordance in landscape genetic patterning. Stochastic mtDNA lineage sorting can be rejected because the mtDNA lineages are essentially distinct geographically for > 1500 km. Vicariance is unlikely: the Great Dividing Range is neither a current barrier nor was it at the Last Glacial Maximum according to species distribution modeling; nuclear gene flow inferred from coalescent analysis affirms this. Female philopatry contradicts known female‐biased dispersal. Contrasting mtDNA and nDNA demographies indicate their evolutionary histories are decoupled. Distance‐based redundancy analysis, in which environmental temperatures explain mtDNA variance above that explained by geographic position and isolation‐by‐distance, favors a nonneutral explanation for mitochondrial phylogeographic patterning. Thus, observed mito‐nuclear discordance accords with environmental selection on a female‐linked trait, such as mtDNA, mtDNA–nDNA interactions or genes on W‐chromosome, driving mitochondrial divergence in the presence of nuclear gene flow.

Mitochondrial phylogeographies of five widespread Eurasian bird species

Five species of Eurasian birds displayed a range of mitochondrial DNA phylogeographic structures, including a single widespread lineage (common sandpiper), two geographically unsorted and closely related lineages (long-tailed tit), three partially overlapping closely related lineages (reed bunting), and two divergent geographically isolated lineages that rival species distinction (red-breasted flycatcher and skylark). Only the red-breasted flycatcher and the skylark displayed congruent phylogeographic structures. These five species represent different stages of diversification and speciation. There was little evidence that natural selection had influenced mitochondrial NADH dehydrogenase subunit 2 (ND2) sequences. In several instances, population growth was hypothesized, based on haplotype distributions within populations.

Predicting landscape-genetic consequences of habitat loss, fragmentation and mobility for multiple species of woodland birds.

Inference concerning the impact of habitat fragmentation on dispersal and gene flow is a key theme in landscape genetics. Recently, the ability of established approaches to identify reliably the differential effects of landscape structure (e.g. land-cover composition, remnant vegetation configuration and extent) on the mobility of organisms has been questioned. More explicit methods of predicting and testing for such effects must move beyond post hoc explanations for single landscapes and species. Here, we document a process for making a priori predictions, using existing spatial and ecological data and expert opinion, of the effects of landscape structure on genetic structure of multiple species across replicated landscape blocks. We compare the results of two common methods for estimating the influence of landscape structure on effective distance: least-cost path analysis and isolation-by-resistance. We present a series of alternative models of genetic connectivity in the study area, represented by different landscape resistance surfaces for calculating effective distance, and identify appropriate null models. The process is applied to ten species of sympatric woodland-dependant birds. For each species, we rank a priori the expectation of fit of genetic response to the models according to the expected response of birds to loss of structural connectivity and landscape-scale tree-cover. These rankings (our hypotheses) are presented for testing with empirical genetic data in a subsequent contribution. We propose that this replicated landscape, multi-species approach offers a robust method for identifying the likely effects of landscape fragmentation on dispersal.

Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance

Diversifying selection on metabolic pathways can reduce intraspecific gene flow and promote population divergence. An opportunity to explore this arises from mitonuclear discordance observed in an Australian bird Eopsaltria australis. Across >1500 km, nuclear differentiation is low and latitudinally structured by isolation by distance, whereas two highly divergent, parapatric mitochondrial lineages (>6.6% in ND2) show a discordant longitudinal geographic pattern and experience different climates. Vicariance, incomplete lineage sorting and sex‐biased dispersal were shown earlier to be unlikely drivers of the mitonuclear discordance; instead, natural selection on a female‐linked trait was the preferred hypothesis. Accordingly, here we tested for signals of positive, divergent selection on mitochondrial genes in E. australis. We used codon models and physicochemical profiles of amino acid replacements to analyse complete mitochondrial genomes of the two mitochondrial lineages in E. australis, its sister species Eopsaltria griseogularis, and outgroups. We found evidence of positive selection on at least five amino acids, encoded by genes of two oxidative phosphorylation pathway complexes NADH dehydrogenase (ND4 and ND4L) and cytochrome bc1 (cyt‐b) against a background of widespread purifying selection on all mitochondrial genes. Three of these amino acid replacements were fixed in ND4 of the geographically most widespread E. australis lineage. The other two replacements were fixed in ND4L and cyt‐b of the geographically more restricted E. australis lineage. We discuss whether this selection may reflect local environmental adaptation, a by‐product of other selective processes, or genetic incompatibilities, and propose how these hypotheses can be tested in future.

Barn swallows before barns: population histories and intercontinental colonization.

The barn swallow (Hirundo rustica) is one of most widely distributed swallows, owing in part to its recent switch from natural nest sites to human structures. We conducted phylogenetic analysis of mitochondrial (mt) and nuclear DNA to explore the recent evolutionary history of this species. Strongly supported mtDNA clades corresponded to Europe, Asia and North America plus the Baikal region of Asia. Analysis of sequence data from a sex-linked nuclear gene was unable to recover the phylogenetic splits in the mtDNA tree, confirming that the main clades evolved recently. The phylogenetic pattern suggests that the ancestral area of the barn swallow was the holarctic; most divergence events are consistent with vicariance. Most unexpectedly, analyses show that barn swallows from North America colonized the Baikal region in the recent past (one fixed substitution). This dispersal direction is opposite of that for most nearctic–palearctic taxon exchanges. Although this invasion was envisioned to coincide with the appearance of new types of human dwelling in the Baikal region, calibration of molecular divergence suggests an older dispersal event. A recent history of gene flow within the main palearctic clades is consistent with range and population expansion owing to new nesting opportunities provided by human settlements. Contrary to expectation, populations in North America appear historically larger and more stable than those in the palearctic. The Baikal population apparently has not increased greatly since colonization.

Mitochondrial DNA Indicates Late Pleistocene Divergence of Populations of Heteronympha merope, an Emerging Model in Environmental Change Biology

Knowledge of historical changes in species range distribution provides context for investigating adaptive potential and dispersal ability. This is valuable for predicting the potential impact of environmental change on species of interest. Butterflies are one of the most important taxa for studying such impacts, and Heteronympha merope has the potential to provide a particularly valuable model, in part due to the existence of historical data on morphological traits and glycolytic enzyme variation. This study investigates the population genetic structure and phylogeography of H. merope, comparing the relative resolution achieved through partial DNA sequences of two mitochondrial loci, COI and ND5. These data are used to define the relationship between subspecies, showing that the subspecies are reciprocally monophyletic. On this basis, the Western Australian subspecies H. m. duboulayi is genetically distinct from the two eastern subspecies. Throughout the eastern part of the range, levels of migration and the timing of key population splits of potential relevance to climatic adaptation are estimated and indicate Late Pleistocene divergence both of the Tasmanian subspecies and of an isolated northern population from the eastern mainland subspecies H. m. merope. This information is then used to revisit historical data and provides support for the importance of clinal variation in wing characters, as well as evidence for selective pressure acting on allozyme loci phosphoglucose isomerase and phosphoglucomutase in H. merope. The study has thus confirmed the value of H. merope as a model organism for measuring responses to environmental change, offering the opportunity to focus on isolated populations, as well as a latitudinal gradient, and to use historical changes to test the accuracy of predictions for the future.