S. Elizabeth Alter

DNA evidence for historic population size and past ecosystem impacts of gray whales.

Ecosystem restoration may require returning threatened populations of ecologically pivotal species to near their former abundances, but it is often difficult to estimate historic population size of species that have been heavily exploited. Eastern Pacific gray whales play a key ecological role in their Arctic feeding grounds and are widely thought to have returned to their prewhaling abundance. Recent mortality spikes might signal that the population has reached long-term carrying capacity, but an alternative is that this decline was due to shifting climatic conditions on Arctic feeding grounds. We used a genetic approach to estimate prewhaling abundance of gray whales and report DNA variability at 10 loci that is typical of a population of ≈76,000–118,000 individuals, approximately three to five times more numerous than todays average census size of 22,000. Coalescent simulations indicate these estimates may include the entire Pacific metapopulation, suggesting that our average measurement of ≈96,000 individuals was probably distributed between the eastern and currently endangered western Pacific populations. These levels of genetic variation suggest the eastern population is at most at 28–56% of its historical abundance and should be considered depleted. If used to inform management, this would halve acceptable human-caused mortality for this population from 417 to 208 per year. Potentially profound ecosystem impacts may have resulted from a decline from 96,000 gray whales to the current population. At previous levels, gray whales may have seasonally resuspended 700 million cubic meters of sediment, as much as 12 Yukon Rivers, and provided food to a million sea birds.

Pre-whaling genetic diversity and population ecology in eastern Pacific gray whales: insights from ancient DNA and stable isotopes.

Commercial whaling decimated many whale populations, including the eastern Pacific gray whale, but little is known about how population dynamics or ecology differed prior to these removals. Of particular interest is the possibility of a large population decline prior to whaling, as such a decline could explain the ∼5-fold difference between genetic estimates of prior abundance and estimates based on historical records. We analyzed genetic (mitochondrial control region) and isotopic information from modern and prehistoric gray whales using serial coalescent simulations and Bayesian skyline analyses to test for a pre-whaling decline and to examine prehistoric genetic diversity, population dynamics and ecology. Simulations demonstrate that significant genetic differences observed between ancient and modern samples could be caused by a large, recent population bottleneck, roughly concurrent with commercial whaling. Stable isotopes show minimal differences between modern and ancient gray whale foraging ecology. Using rejection-based Approximate Bayesian Computation, we estimate the size of the population bottleneck at its minimum abundance and the pre-bottleneck abundance. Our results agree with previous genetic studies suggesting the historical size of the eastern gray whale population was roughly three to five times its current size.

Comparing evolutionary patterns and variability in the mitochondrial control region and cytochrome B in three species of baleen whales.

The rapidly evolving mitochondrial control region remains an important source of information on phylogeography and demographic history for cetaceans and other vertebrates, despite great uncertainty in the rate of nucleotide substitution across both nucleotide positions and lineages. Patterns of variation in linked markers with slower rates of evolution can potentially be used to calibrate the rate of nucleotide substitution in the control region and to better understand the interplay of evolutionary and demographic forces across the mitochondrial genome above and below the species level. We have examined patterns of diversity within and between three baleen whale species (gray, humpback, and Antarctic minke whales) in order to determine how patterns of molecular evolution differ between cytochrome b and the control region. Our results show that cytochrome b is less variable than expected given the diversity in the control region for gray and humpback whales, even after functional differences are taken into account, but more variable than expected for minke whales. Differences in the frequency distributions of polymorphic sites and in best-fit models of nucleotide substitution indicate that these patterns may be the result of hypervariability in the control region in gray and humpback whales but, in minke whales, may result from a large, stable or expanding population size coupled with saturation at the control region. Using paired cytochrome b and control region data across individuals, we show that the average rate of nucleotide substitution in the control region may be on average 2.6 times higher than phylogenetically derived estimates in cetaceans. These results highlight the complexity of making inferences from control region data alone and suggest that applying simple rules of DNA sequence analyses across species may be difficult.

Gene flow on ice: the role of sea ice and whaling in shaping Holarctic genetic diversity and population differentiation in bowhead whales (Balaena mysticetus)

Sea ice is believed to be a major factor shaping gene flow for polar marine organisms, but it remains unclear to what extent it represents a true barrier to dispersal for arctic cetaceans. Bowhead whales are highly adapted to polar sea ice and were targeted by commercial whalers throughout Arctic and subarctic seas for at least four centuries, resulting in severe reductions in most areas. Both changing ice conditions and reductions due to whaling may have affected geographic distribution and genetic diversity throughout their range, but little is known about range-wide genetic structure or whether it differed in the past. This study represents the first examination of genetic diversity and differentiation across all five putative stocks, including Baffin Bay-Davis Strait, Hudson Bay-Foxe Basin, Bering-Beaufort-Chukchi, Okhotsk, and Spitsbergen. We also utilized ancient specimens from Prince Regent Inlet (PRI) in the Canadian Arctic and compared them with modern stocks. Results from analysis of molecular variance and demographic simulations are consistent with recent and high gene flow between Atlantic and Pacific stocks in the recent past. Significant genetic differences between ancient and modern populations suggest PRI harbored unique maternal lineages in the past that have been recently lost, possibly due to loss of habitat during the Little Ice Age and/or whaling. Unexpectedly, samples from this location show a closer genetic relationship with modern Pacific stocks than Atlantic, supporting high gene flow between the central Canadian Arctic and Beaufort Sea over the past millennium despite extremely heavy ice cover over much of this period.

Mitochondrial and Nuclear Genetic Variation across Calving Lagoons in Eastern North Pacific Gray Whales (Eschrichtius robustus)

Accurate knowledge of population structure in cetaceans is critical for preserving and managing breeding habitat, particularly when habitat is not uniformly protected. Most eastern gray whales return to their major breeding range each winter along the Pacific coast of Baja California, Mexico, concentrating in 3 major calving lagoons, but it is unknown whether genetic differences exist between lagoons. Previous photo-identification studies and genetic studies suggest that gray whales may return to their natal lagoons to breed, potentially resulting in the buildup of genetic differences. However, an earlier genetic study used only one genetic marker and did not include samples from Bahia Magdalena, a major calving lagoon not currently designated as a wildlife refuge. To expand on this previous study, we collected genetic data from the mitochondrial control region (442 bp) and 9 microsatellite markers from 112 individuals across all 3 major calving lagoons. Our data suggest that migration rates between calving lagoons are high but that a small but significant departure from panmixia exists between Bahia Magdalena and Laguna San Ignacio (Fishers Exact test, P < 0.0001; F(ST) = 0.006, P = 0.025). Coalescent simulations show that the lack of extensive population structure may result from the disruption of structure due to whaling. Another possibility is that rates of migration have always been high (>10% per generation). In addition, microsatellite data showed evidence of a severe population bottleneck. Eastern gray whales are still recovering from the impacts of whaling on their breeding grounds, and these populations should be protected and monitored for future genetic changes.

Genomewide SNP data reveal cryptic phylogeographic structure and microallopatric divergence in a rapids-adapted clade of cichlids from the Congo River

The lower Congo River is a freshwater biodiversity hot spot in Africa characterized by some of the worlds largest rapids. However, little is known about the evolutionary forces shaping this diversity, which include numerous endemic fishes. We investigated phylogeographic relationships in Teleogramma, a small clade of rheophilic cichlids, in the context of regional geography and hydrology. Previous studies have been unable to resolve phylogenetic relationships within Teleogramma due to lack of variation in nuclear genes and discrete morphological characters among putative species. To sample more broadly across the genome, we analysed double‐digest restriction‐associated sequencing (ddRAD) data from 53 individuals across all described species in the genus. We also assessed body shape and mitochondrial variation within and between taxa. Phylogenetic analyses reveal previously unrecognized lineages and instances of microallopatric divergence across as little as ~1.5 km. Species ranges appear to correspond to geographic regions broadly separated by major hydrological and topographic barriers, indicating these features are likely important drivers of diversification. Mitonuclear discordance indicates one or more introgressive hybridization events, but no clear evidence of admixture is present in nuclear genomes, suggesting these events were likely ancient. A survey of female fin patterns hints that previously undetected lineage‐specific patterning may be acting to reinforce species cohesion. These analyses highlight the importance of hydrological complexity in generating diversity in certain freshwater systems, as well as the utility of ddRAD‐Seq data in understanding diversification processes operating both below and above the species level.

Phylogenetics of Teleogramma, a Riverine Clade of African Cichlid Fishes, with a Description of the Deepwater Molluskivore—Teleogramma obamaorum— from the Lower Reaches of the Middle Congo River

ABSTRACT The lower Congo River and nearby habitats harbor numerous endemic lineages of cichlid fishes, including some with highly specialized morphologies. Based on morphological and molecular data, we herein describe a new species of Teleogramma, a member of the chromidotilapiine clade found on rocky outcrops in the lower reaches of the middle Congo River. The new species, T. obamaorum, is distinguished from congeners by numerous morphological and ecological attributes, including the lack of dorsoventral head and body depression, absence of sexual dichromatism, and features of laterosensory anatomy, pharyngeal and gut morphology, and dietary preference. Phylogenetic analyses of two nuclear and two mitochondrial loci using Bayesian and maximum-likelihood inference lend strong support for the taxonomic validity of T. obamaorum and provide preliminary estimates of species relationships within the genus. The discovery of a new, ecomorphologically distinctive cichlid species in the Congo River suggests that additional research focus on riverine clades has the potential to greatly contribute to our understanding of evolutionary dynamics in this hyperdiverse group of teleost fishes.

Fishes in the desert: mitochondrial variation and phylogeography of Danakilia (Actinopterygii: Cichlidae) and Aphanius (Actinopterygii: Cyprinodontidae) in the Danakil Depression of northeastern Africa

Abstract The Danakil Depression in northeastern Africa represents one of the harshest arid environments on Earth, yet two genera of fishes, Danakilia (Cichlidae) and Aphanius (Cyprinodontidae), share its sparse aquatic habitats. The evolutionary history of these fishes is investigated here in the context of genetic, geological and paleoenvironmental information. We collected samples from seven sites and assessed phylogeographic relationships using concatenated COI and cytb mtDNA genes. Danakilia morphospecies show low differentiation at mitochondrial markers, but variation is partitioned between a northern cluster containing D. dinicolai plus three undescribed riverine populations, and a southern cluster including two creek populations of D. franchettii separated by the hypersaline waters of Lake Afrera. Aphanius displayed four genetically distinct clades (A. stiassnyae in Lake Afrera; one distributed across the entire area; one in Lake Abaeded; and one in the Shukoray River), but without clear large-scale geographic structure. However, Danakil Aphanius are clearly differentiated from A. dispar sensu stricto from the Sinai Peninsula. Geological evidence suggests that after the Late Pleistocene closure of the Danakil-Red Sea connection, increased post-glacial groundwater availability caused the formation of a brackish paleo-lake flooding the entire region below the –50 m contour. Fish populations previously isolated in coastal oases during glaciation were able to mix in the paleo-lake. Subsequently, in a more arid phase starting ∼7300 BP, paleo-lake regression isolated fishes in separate drainages, triggering their still ongoing diversification.

Melting Barriers to Faunal Exchange Across Ocean Basins

Accelerated loss of sea ice in the Arctic is opening routes connecting the Atlantic and Pacific Oceans for longer periods each year. These changes may increase the ease and frequency with which marine birds and mammals move between the Pacific and Atlantic Ocean basins. Indeed, recent observations of birds and mammals suggest these movements have intensified in recent decades. Reconnection of the Pacific and Atlantic Ocean basins will present both challenges to marine ecosystem conservation and an unprecedented opportunity to examine the ecological and evolutionary consequences of interoceanic faunal exchange in real time. To understand these changes and implement effective conservation of marine ecosystems, we need to further develop modeling efforts to predict the rate of dispersal and consequences of faunal exchange. These predictions can be tested by closely monitoring wildlife dispersal through the Arctic Ocean and using modern methods to explore the ecological and evolutionary consequences of these movements.

First genome‐wide analysis of the endangered, endemic lichen Cetradonia linearis reveals isolation by distance and strong population structure

PREMISE OF THE STUDY Lichenized fungi are evolutionarily diverse and ecologically important, but little is known about the processes that drive their diversification and genetic differentiation. Distributions are often assumed to be wholly shaped by ecological requirements rather than dispersal limitations. Furthermore, although asexual and sexual reproductive structures are observable, the lack of information about recombination rates makes inferences about reproductive strategies difficult. We investigated the population genomics of Cetradonia linearis, a federally endangered lichen in the southern Appalachians of eastern North America, to test the relative contributions of environmental and geographic distance in shaping genetic structure, and to characterize the mating system and genome-wide recombination. METHODS Whole-genome shotgun sequencing was conducted to generate data for 32 individuals of C. linearis. A reference genome was assembled, and reads from all samples were aligned to generate a set of single-nucleotide polymorphisms for further analyses. KEY RESULTS We found evidence for low rates of recombination and for isolation by distance, but not for isolation by environment. The species is putatively unisexual, given that only one mating-type locus was found. Hindcast species distribution models and the distribution of genetic diversity support C. linearis having a larger range during the Last Glacial Maximum in the southern portion of its current extent. CONCLUSIONS Our findings contribute to the understanding of factors that shape genetic diversity in C. linearis and in fungi more broadly. Because all populations are highly genetically differentiated, the extirpation of any population would mean the loss of unique genetic diversity; therefore, our results support the continued conservation of this species.