Population genomics and conservation management of a declining tropical rodent

Conservation management is improved by incorporating information about the spatial distribution of population genetic diversity into planning strategies. Northern Australia is the location of some of the world’s most severe ongoing declines of endemic mammal species, yet we have little genetic information from this regional mammal assemblage to inform a genetic perspective on conservation assessment and planning. We used next-generation sequencing data from remnant populations of the threatened brush-tailed rabbit-rat (Conilurus penicillatus) to compare patterns of genomic diversity and differentiation across the landscape and investigate standardised hierarchical genomic diversity metrics to better understand brush-tailed rabbit-rat population genomic structure. We found strong population structuring, with high levels of differentiation between populations (F_ST = 0.21–0.78). Two distinct genomic lineages between the Tiwi Islands and mainland are also present. Prioritisation analysis showed that one population in both lineages would need to be conserved to retain at least ~80% of alleles for the species. Analysis of standardised genomic diversity metrics showed that approximately half of the total diversity occurs among lineages (δ = 0.091 from grand total γ = 0.184). We suggest that a focus on conserving remnant island populations may not be appropriate for the preservation of species-level genomic diversity and adaptive potential, as these populations represent a small component of the total diversity and a narrow subset of the environmental conditions in which the species occurs. We also highlight the importance of considering both genomic and ecological differentiation between source and receiving populations when considering translocations for conservation purposes.Subject terms: Ecological genetics, Population genetics, Conservation biology, Biogeography     

Morphological and Genetic Divergences in a Coral Reef Damselfish, Pomacentrus coelestis

Population differentiation is one of the main topics in evolutionary biology. Except the exploration of color variation, few studies focused on morphological divergences among populations of coral reef fishes. In this work, we studied morphological and genetic differentiation among populations of the damselfish, Pomacentrus coelestis, in the northwestern Pacific Ocean. The shapes of the mandible and the premaxilla were explored using geometric morphometric methods and the genetic structure was investigated using microsattelites. Various tests revealed significant shape variation among most P. coelestis populations for both skeletal units. Morphological variation of the mandible accompanies a genetic break between populations of mainland Japan and Okinawa-Taiwan. However, Mantel and Procrustes tests revealed no congruence between morphological and genetic structures. We illustrate that phenotypic plasticity and adaptive divergence are potential evolutionary mechanisms underlying shape difference among P. coelestis populations. An ecomorphological approach suggests that various diet could be related to shape variation of oral jaws.     

Birds are islands for parasites

Understanding the mechanisms driving the extraordinary diversification of parasites is a major challenge in evolutionary biology. Co-speciation, one proposed mechanism that could contribute to this diversity is hypothesized to result from allopatric co-divergence of host–parasite populations. We found that island populations of the Galápagos hawk (Buteo galapagoensis) and a parasitic feather louse species (Degeeriella regalis) exhibit patterns of co-divergence across variable temporal and spatial scales. Hawks and lice showed nearly identical population genetic structure across the Galápagos Islands. Hawk population genetic structure is explained by isolation by distance among islands. Louse population structure is best explained by hawk population structure, rather than isolation by distance per se, suggesting that lice tightly track the recent population histories of their hosts. Among hawk individuals, louse populations were also highly structured, suggesting that hosts serve as islands for parasites from an evolutionary perspective. Altogether, we found that host and parasite populations may have responded in the same manner to geographical isolation across spatial scales. Allopatric co-divergence is likely one important mechanism driving the diversification of parasites.     

A Two-Locus System with Strong Epistasis Underlies Rapid Parasite-Mediated Evolution of Host Resistance

Parasites are a major evolutionary force, driving adaptive responses in host populations. Although the link between phenotypic response to parasite-mediated natural selection and the underlying genetic architecture often remains obscure, this link is crucial for understanding the evolution of resistance and predicting associated allele frequency changes in the population. To close this gap, we monitored the response to selection during epidemics of a virulent bacterial pathogen, Pasteuria ramosa, in a natural host population of Daphnia magna. Across two epidemics, we observed a strong increase in the proportion of resistant phenotypes as the epidemics progressed. Field and laboratory experiments confirmed that this increase in resistance was caused by selection from the local parasite. Using a genome-wide association study, we built a genetic model in which two genomic regions with dominance and epistasis control resistance polymorphism in the host. We verified this model by selfing host genotypes with different resistance phenotypes and scoring their F1 for segregation of resistance and associated genetic markers. Such epistatic effects with strong fitness consequences in host–parasite coevolution are believed to be crucial in the Red Queen model for the evolution of genetic recombination.     

Genomic and phenotypic differentiation among Methanosarcina mazei populations from Columbia River sediment

Methanogenic archaea are genotypically and phenotypically diverse organisms that are integral to carbon cycling in anaerobic environments. Owing to their genetic tractability and ability to be readily cultivated, Methanosarcina spp. have become a powerful model system for understanding methanogen biology at the cellular systems level. However, relatively little is known of how genotypic and phenotypic variation is partitioned in Methanosarcina populations inhabiting natural environments and the possible ecological and evolutionary implications of such variation. Here, we have identified how genomic and phenotypic diversity is partitioned within and between Methanosarcina mazei populations obtained from two different sediment environments in the Columbia River Estuary (Oregon, USA). Population genomic analysis of 56 M. mazei isolates averaging <1% nucleotide divergence revealed two distinct clades, which we refer to as ‘mazei-T'' and ‘mazei-WC''. Genomic analyses showed that these clades differed in gene content and fixation of allelic variants, which point to potential differences in primary metabolism and also interactions with foreign genetic elements. This hypothesis of niche partitioning was supported by laboratory growth experiments that revealed significant differences in trimethylamine utilization. These findings improve our understanding of the ecologically relevant scales of genomic variation in natural systems and demonstrate interactions between genetic and ecological diversity in these easily cultivable and genetically tractable model methanogens.     

Population genomics reveals multiple drivers of population differentiation in a sex‐role‐reversed pipefish

A major goal of molecular ecology is to identify the causes of genetic and phenotypic differentiation among populations. Population genomics is suitably poised to tackle these key questions by diagnosing the evolutionary mechanisms driving divergence in nature. Here, we set out to investigate the evolutionary processes underlying population differentiation in the Gulf pipefish, Syngnathus scovelli. We sampled approximately 50 fish from each of 12 populations distributed from the Gulf coast of Texas to the Atlantic coast of Florida and performed restriction‐site‐associated DNA sequencing to identify SNPs throughout the genome. After imposing quality and stringency filters, we selected a panel of 6348 SNPs present in all 12 populations, 1753 of which were not physically linked. We identified a genome‐wide pattern of isolation by distance, in addition to a more substantial genetic break separating populations in the Gulf of Mexico from those in the Atlantic. We also used several divergence outlier approaches and tests for genotype–environment correlations to identify 400 SNPs putatively involved in local adaptation. Patterns of phenotypic differentiation and variation diverged from the overall genomic pattern, suggesting that selection, phenotypic plasticity or demographic factors may be shaping phenotypes in distinct populations. Overall, our results suggest that population divergence is driven by a variety of factors in S. scovelli, including neutral processes and selection on multiple traits.     

Host plant associations and geography interact to shape diversification in a specialist insect herbivore

Disentangling the processes underlying geographic and environmental patterns of biodiversity challenges biologists as such patterns emerge from eco‐evolutionary processes confounded by spatial autocorrelation among sample units. The herbivorous insect, Belonocnema treatae (Hymenoptera: Cynipidae), exhibits regional specialization on three plant species whose geographic distributions range from sympatry through allopatry across the southern United States. Using range‐wide sampling spanning the geographic ranges of the three host plants and genotyping‐by‐sequencing of 1,217 individuals, we tested whether this insect herbivore exhibited host plant‐associated genomic differentiation while controlling for spatial autocorrelation among the 58 sample sites. Population genomic structure based on 40,699 SNPs was evaluated using the hierarchical Bayesian model entropy to assign individuals to genetic clusters and estimate admixture proportions. To control for spatial autocorrelation, distance‐based Moran's eigenvector mapping was used to construct regression variables summarizing spatial structure inherent among sample sites. Distance‐based redundancy analysis (dbRDA) incorporating the spatial variables was then applied to partition host plant‐associated differentiation (HAD) from spatial autocorrelation. By combining entropy and dbRDA to analyse SNP data, we unveiled a complex mosaic of highly structured differentiation within and among gall‐former populations finding evidence that geography, HAD and spatial autocorrelation all play significant roles in explaining patterns of genomic differentiation in B. treatae. While dbRDA confirmed host association as a significant predictor of patterns of genomic variation, spatial autocorrelation among sites explained the largest proportion of variation. Our results demonstrate the value of combining dbRDA with hierarchical structural analyses to partition spatial/environmental patterns of genomic variation.     

Description of a New Galapagos Giant Tortoise Species (Chelonoidis; Testudines: Testudinidae) from Cerro Fatal on Santa Cruz Island

The taxonomy of giant Galapagos tortoises (Chelonoidis spp.) is currently based primarily on morphological characters and island of origin. Over the last decade, compelling genetic evidence has accumulated for multiple independent evolutionary lineages, spurring the need for taxonomic revision. On the island of Santa Cruz there is currently a single named species, C. porteri. Recent genetic and morphological studies have shown that, within this taxon, there are two evolutionarily and spatially distinct lineages on the western and eastern sectors of the island, known as the Reserva and Cerro Fatal populations, respectively. Analyses of DNA from natural populations and museum specimens, including the type specimen for C. porteri, confirm the genetic distinctiveness of these two lineages and support elevation of the Cerro Fatal tortoises to the rank of species. In this paper, we identify DNA characters that define this new species, and infer evolutionary relationships relative to other species of Galapagos tortoises.     

Maximum antigen diversification in a lyme bacterial population and evolutionary strategies to overcome pathogen diversity

Natural populations of pathogens and their hosts are engaged in an arms race in which the pathogens diversify to escape host immunity while the hosts evolve novel immunity. This co-evolutionary process poses a fundamental challenge to the development of broadly effective vaccines and diagnostics against a diversifying pathogen. Based on surveys of natural allele frequencies and experimental immunization of mice, we show high antigenic specificities of natural variants of the outer surface protein C (OspC), a dominant antigen of a Lyme Disease-causing bacterium (Borrelia burgdorferi). To overcome the challenge of OspC antigenic diversity to clinical development of preventive measures, we implemented a number of evolution-informed strategies to broaden OspC antigenic reactivity. In particular, the centroid algorithm—a genetic algorithm to generate sequences that minimize amino-acid differences with natural variants—generated synthetic OspC analogs with the greatest promise as diagnostic and vaccine candidates against diverse Lyme pathogen strains co-existing in the Northeast United States. Mechanistically, we propose a model of maximum antigen diversification (MAD) mediated by amino-acid variations distributed across the hypervariable regions on the OspC molecule. Under the MAD hypothesis, evolutionary centroids display broad cross-reactivity by occupying the central void in the antigenic space excavated by diversifying natural variants. In contrast to vaccine designs based on concatenated epitopes, the evolutionary algorithms generate analogs of natural antigens and are automated. The novel centroid algorithm and the evolutionary antigen designs based on consensus and ancestral sequences have broad implications for combating diversifying pathogens driven by pathogen–host co-evolution.Subject terms: Population genetics, Bacterial genetics     

Genomic diversity and differentiation of a managed island wild boar population

The evolution of island populations in natural systems is driven by local adaptation and genetic drift. However, evolutionary pathways may be altered by humans in several ways. The wild boar (WB) (Sus scrofa) is an iconic game species occurring in several islands, where it has been strongly managed since prehistoric times. We examined genomic diversity at 49 803 single-nucleotide polymorphisms in 99 Sardinian WBs and compared them with 196 wild specimens from mainland Europe and 105 domestic pigs (DP; 11 breeds). High levels of genetic variation were observed in Sardinia (80.9% of the total number of polymorphisms), which can be only in part associated to recent genetic introgression. Both Principal Component Analysis and Bayesian clustering approach revealed that the Sardinian WB population is highly differentiated from the other European populations (F_ST=0.126–0.138), and from DP (F_ST=0.169). Such evidences were mostly unaffected by an uneven sample size, although clustering results in reference populations changed when the number of individuals was standardized. Runs of homozygosity (ROHs) pattern and distribution in Sardinian WB are consistent with a past expansion following a bottleneck (small ROHs) and recent population substructuring (highly homozygous individuals). The observed effect of a non-random selection of Sardinian individuals on diversity, F_ST and ROH estimates, stressed the importance of sampling design in the study of structured or introgressed populations. Our results support the heterogeneity and distinctiveness of the Sardinian population and prompt further investigations on its origins and conservation status.     

Gene Flow and Genetic Diversity of a Broadcast-Spawning Coral in Northern Peripheral Populations

Recently, reef-building coral populations have been decreasing worldwide due to various disturbances. Population genetic studies are helpful for estimating the genetic connectivity among populations of marine sessile organisms with metapopulation structures such as corals. Moreover, the relationship between latitude and genetic diversity is informative when evaluating the fragility of populations. In this study, using highly variable markers, we examined the population genetics of the broadcast-spawning coral Acropora digitifera at 19 sites in seven regions along the 1,000 km long island chain of Nansei Islands, Japan. This area includes both subtropical and temperate habitats. Thus, the coral populations around the Nansei Islands in Japan are northern peripheral populations that would be subjected to environmental stresses different from those in tropical areas. The existence of high genetic connectivity across this large geographic area was suggested for all sites (F _ST≤0.033) although small but significant genetic differentiation was detected among populations in geographically close sites and regions. In addition, A. digitifera appears to be distributed throughout the Nansei Islands without losing genetic diversity. Therefore, A. digitifera populations in the Nansei Islands may be able to recover relatively rapidly even when high disturbances of coral communities occur locally if populations on other reefs are properly maintained.     

Molecular population genetics of the OBP83 genomic region in Drosophila subobscura and D. guanche: contrasting the effects of natural selection and gene arrangement expansion in the patterns of nucleotide variation

Chromosomal inversion polymorphism play a major role in the evolutionary dynamics of populations and species because of their effects on the patterns of genetic variability in the genomic regions within inversions. Though there is compelling evidence for the adaptive character of chromosomal polymorphisms, the mechanisms responsible for their maintenance in natural populations is not fully understood. For this type of analysis, Drosophila subobscura is a good model species as it has a rich and extensively studied chromosomal inversion polymorphism system. Here, we examine the patterns of DNA variation in two natural populations segregating for chromosomal arrangements that differentially affect the surveyed genomic region; in particular, we analyse both nucleotide substitutions and insertion/deletion variations in the genomic region encompassing the odorant-binding protein genes Obp83a and Obp83b (Obp83 region). We show that the two main gene arrangements are genetically differentiated, but are consistent with a monophyletic origin of inversions. Nevertheless, these arrangements interchange some genetic information, likely by gene conversion. We also find that the frequency spectrum-based tests indicate that the pattern of nucleotide variation is not at equilibrium; this feature probably reflects the rapid increase in the frequency of the new gene arrangement promoted by positive selection (that is an adaptive change). Furthermore, a comparative analysis of polymorphism and divergence patterns reveals a relaxation of the functional constraints at the Obp83b gene, which might be associated with particular ecological or demographic features of the Canary island endemic species D. guanche     

Microevolutionary dynamics of a macroevolutionary key innovation in a Lepidopteran herbivore

Background  

A molecular population genetics understanding is central to the study of ecological and evolutionary functional genomics. Population genetics identifies genetic variation and its distribution within and among populations, it reveals the demographic history of the populations studied, and can provide indirect insights into historical selection dynamics. Here we use this approach to examine the demographic and selective dynamics acting of a candidate gene involved in plant-insect interactions. Previous work documents the macroevolutionary and historical ecological importance of the nitrile-specifier protein (Nsp), which facilitated the host shift of Pieridae butterflies onto Brassicales host plants ~80 Myr ago.     

Sequence variation in the Mc1r gene for a group of polymorphic snakes

Studying the genetic factors underlying phenotypic traits can provide insight into dynamics of selection and molecular basis of adaptation, but this goal can be difficult for non-model organisms without extensive genomic resources. However, sequencing candidate genes for the trait of interest can facilitate the study of evolutionary genetics in natural populations. We sequenced the melanocortin-1 receptor (Mc1r) to study the genetic basis of color polymorphism in a group of snake species with variable black banding, the genera Sonora, Chilomeniscus, and Chionactis. Mc1r is an important gene in the melanin synthesis pathway and is associated with ecologically important variation in color pattern in birds, mammals, and other squamate reptiles. We found that Mc1r nucleotide sequence was variable and that within our focal Sonora species, there are both fixed and heterozygous nucleotide substitutions that result in an amino acid change and selection analyses indicated that Mc1r sequence was likely under purifying selection. However, we did not detect any statistical association with the presence or absence of black bands. Our results agree with other studies that have found no role for sequence variation in Mc1r and highlight the importance of comparative data for studying the phenotypic associations of candidate genes.     

Evidence of local adaptation despite strong drift in a Neotropical patchily distributed bromeliad

Both genetic drift and divergent selection are predicted to be drivers of population differentiation across patchy habitats, but the extent to which these forces act on natural populations to shape traits is strongly affected by species’ ecological features. In this study, we infer the genomic structure of Pitcairnia lanuginosa, a widespread herbaceous perennial plant with a patchy distribution. We sampled populations in the Brazilian Cerrado and the Central Andean Yungas and discovered and genotyped SNP markers using double-digest restriction-site associated DNA sequencing. In addition, we analyzed ecophysiological traits obtained from a common garden experiment and compared patterns of phenotypic and genetic divergence (P_ST–F_ST comparisons) in a subset of populations from the Cerrado. Our results from molecular analyses pointed to extremely low genetic diversity and a remarkable population differentiation, supporting a major role of genetic drift. Approximately 0.3% of genotyped SNPs were flagged as differentiation outliers by at least two distinct methods, and Bayesian generalized linear mixed models revealed a signature of isolation by environment in addition to isolation by distance for high-differentiation outlier SNPs among the Cerrado populations. P_ST–F_ST comparisons suggested divergent selection on two ecophysiological traits linked to drought tolerance. We showed that these traits vary among populations, although without any particular macro-spatial pattern, suggesting local adaptation to differences in micro-habitats. Our study shows that selection might be a relevant force, particularly for traits involved in drought stress, even for populations experiencing strong drift, which improves our knowledge on eco-evolutionary processes acting on non-continuously distributed species.Subject terms: Population genetics, Speciation     

Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa

Genetic variation among hosts for resistance to parasites is an important assumption underlying evolutionary theory of host and parasite evolution. Using the castrating bacterial parasite Pasteuria ramosa and its cladoceran host Daphnia magna, we examined both within- and between-population genetic variation for resistance. First, we tested hosts from four populations for genetic variation for resistance to three parasite isolates. Allozyme analysis revealed significant host population divergence and that genetic distance corresponds to geographic distance. Host and parasite fitness components showed strong genetic differences between parasite isolates for host population by parasite interactions and for clones within populations, whereas host population effects were significant for only a few traits. In a second experiment we tested explicitly for within-population differences in variation for resistance by challenging nine host clones from a single population with four different parasite spore doses. Strong clone and dose effects were evident. More susceptible clones also suffered higher costs once infected. The results indicate that within-population variation for resistance is high relative to between-population variation. We speculate that P. ramosa adapts to individual host clones rather than to its host population.     

Host ecotype generates evolutionary and epidemiological divergence across a pathogen metapopulation

The extent and speed at which pathogens adapt to host resistance varies considerably. This presents a challenge for predicting when—and where—pathogen evolution may occur. While gene flow and spatially heterogeneous environments are recognized to be critical for the evolutionary potential of pathogen populations, we lack an understanding of how the two jointly shape coevolutionary trajectories between hosts and pathogens. The rust pathogen Melampsora lini infects two ecotypes of its host plant Linum marginale that occur in close proximity yet in distinct populations and habitats. In this study, we found that within-population epidemics were different between the two habitats. We then tested for pathogen local adaptation at host population and ecotype level in a reciprocal inoculation study. Even after controlling for the effect of spatial structure on infection outcome, we found strong evidence of pathogen adaptation at the host ecotype level. Moreover, sequence analysis of two pathogen infectivity loci revealed strong genetic differentiation by host ecotype but not by distance. Hence, environmental variation can be a key determinant of pathogen population genetic structure and coevolutionary dynamics and can generate strong asymmetry in infection risks through space.     

Genomic Consequences of Long-Term Population Decline in Brown Eared Pheasant

Population genetic theory and empirical evidence indicate that deleterious alleles can be purged in small populations. However, this viewpoint remains controversial. It is unclear whether natural selection is powerful enough to purge deleterious mutations when wild populations continue to decline. Pheasants are terrestrial birds facing a long-term risk of extinction as a result of anthropogenic perturbations and exploitation. Nevertheless, there are scant genomics resources available for conservation management and planning. Here, we analyzed comparative population genomic data for the three extant isolated populations of Brown eared pheasant (Crossoptilon mantchuricum) in China. We showed that C. mantchuricum has low genome-wide diversity and a contracting effective population size because of persistent declines over the past 100,000 years. We compared genome-wide variation in C. mantchuricum with that of its closely related sister species, the Blue eared pheasant (C. auritum) for which the conservation concern is low. There were detrimental genetic consequences across all C. mantchuricum genomes including extended runs of homozygous sequences, slow rates of linkage disequilibrium decay, excessive loss-of-function mutations, and loss of adaptive genetic diversity at the major histocompatibility complex region. To the best of our knowledge, this study is the first to perform a comprehensive conservation genomic analysis on this threatened pheasant species. Moreover, we demonstrated that natural selection may not suffice to purge deleterious mutations in wild populations undergoing long-term decline. The findings of this study could facilitate conservation planning for threatened species and help recover their population size.     

Phylogeography of a widely distributed plant species reveals cryptic genetic lineages with parallel phenotypic responses to warming and drought conditions

To predict how widely distributed species will perform under future climate change, it is crucial to understand and reveal their underlying phylogenetics. However, detailed information about plant adaptation and its genetic basis and history remains scarce and especially widely distributed species receive little attention despite their putatively high adaptability.To examine the adaptation potential of a widely distributed species, we sampled the model plant Silene vulgaris across Europe. In a greenhouse experiment, we exposed the offspring of these populations to a climate change scenario for central Europe and revealed the population structure through whole‐genome sequencing. Plants were grown under two temperatures (18°C and 21°C) and three precipitation regimes (65, 75, and 90 mm) to measure their response in biomass and fecundity‐related traits. To reveal the population genetic structure, ddRAD sequencing was employed for a whole‐genome approach. We found three major genetic clusters in S. vulgaris from Europe: one cluster comprising Southern European populations, one cluster of Western European populations, and another cluster containing central European populations. Population genetic diversity decreased with increasing latitude, and a Mantel test revealed significant correlations between F _ST and geographic distances as well as between genetic and environmental distances. Our trait analysis showed that the genetic clusters significantly differed in biomass‐related traits and in the days to flowering. However, half of the traits showed parallel response patterns to the experimental climate change scenario. Due to the differentiated but parallel response patterns, we assume that phenotypic plasticity plays an important role for the adaptation of the widely distributed species S. vulgaris and its intraspecific genetic lineages.