The 10,000-year biocultural history of fallow deer and its implications for conservation policy.

Over the last 10,000 y, humans have manipulated fallow deer populations with varying outcomes. Persian fallow deer (Dama mesopotamica) are now endangered. European fallow deer (Dama dama) are globally widespread and are simultaneously considered wild, domestic, endangered, invasive and are even the national animal of Barbuda and Antigua. Despite their close association with people, there is no consensus regarding their natural ranges or the timing and circumstances of their human-mediated translocations and extirpations. Our mitochondrial analyses of modern and archaeological specimens revealed two distinct clades of European fallow deer present in Anatolia and the Balkans. Zooarchaeological evidence suggests these regions were their sole glacial refugia. By combining biomolecular analyses with archaeological and textual evidence, we chart the declining distribution of Persian fallow deer and demonstrate that humans repeatedly translocated European fallow deer, sourced from the most geographically distant populations. Deer taken to Neolithic Chios and Rhodes derived not from nearby Anatolia, but from the Balkans. Though fallow deer were translocated throughout the Mediterranean as part of their association with the Greco-Roman goddesses Artemis and Diana, deer taken to Roman Mallorca were not locally available Dama dama, but Dama mesopotamica. Romans also initially introduced fallow deer to Northern Europe but the species became extinct and was reintroduced in the medieval period, this time from Anatolia. European colonial powers then transported deer populations across the globe. The biocultural histories of fallow deer challenge preconceptions about the divisions between wild and domestic species and provide information that should underpin modern management strategies.

Genomics of post-bottleneck recovery in the northern elephant seal.

Populations and species are threatened by human pressure, but their fate is variable. Some depleted populations, such as that of the northern elephant seal (Mirounga angustirostris), recover rapidly even when the surviving population was small. The northern elephant seal was hunted extensively and taken by collectors between the early 1800s and 1892, suffering an extreme population bottleneck as a consequence. Recovery was rapid and now there are over 200,000 individuals. We sequenced 260 modern and 8 historical northern elephant seal nuclear genomes to assess the impact of the population bottleneck on individual northern elephant seals and to better understand their recovery. Here we show that inbreeding, an increase in the frequency of alleles compromised by lost function, and allele frequency distortion, reduced the fitness of breeding males and females, as well as the performance of adult females on foraging migrations. We provide a detailed investigation of the impact of a severe bottleneck on fitness at the genomic level and report on the role of specific gene systems.

Moderating the neutralist-selectionist debate: exactly which propositions are we debating, and which arguments are valid?

Half a century after its foundation, the neutral theory of molecular evolution continues to attract controversy. The debate has been hampered by the coexistence of different interpretations of the core proposition of the neutral theory, the 'neutral mutation-random drift' hypothesis. In this review, we trace the origins of these ambiguities and suggest potential solutions. We highlight the difference between the original, the revised and the nearly neutral hypothesis, and re-emphasise that none of them equates to the null hypothesis of strict neutrality. We distinguish the neutral hypothesis of protein evolution, the main focus of the ongoing debate, from the neutral hypotheses of genomic and functional DNA evolution, which for many species are generally accepted. We advocate a further distinction between a narrow and an extended neutral hypothesis (of which the latter posits that random non-conservative amino acid substitutions can cause non-ecological phenotypic divergence), and we discuss the implications for evolutionary biology beyond the domain of molecular evolution. We furthermore point out that the debate has widened from its initial focus on point mutations, and also concerns the fitness effects of large-scale mutations, which can alter the dosage of genes and regulatory sequences. We evaluate the validity of neutralist and selectionist arguments and find that the tested predictions, apart from being sensitive to violation of underlying assumptions, are often derived from the null hypothesis of strict neutrality, or equally consistent with the opposing selectionist hypothesis, except when assuming molecular panselectionism. Our review aims to facilitate a constructive neutralist-selectionist debate, and thereby to contribute to answering a key question of evolutionary biology: what proportions of amino acid and nucleotide substitutions and polymorphisms are adaptive?

The raw material of evolution.

Estimates of whale mutation rates contribute to understanding evolutionary processes.

Where to now with the evolutionarily significant unit?

The designation of units for conservation has been a necessary but challenging objective since conservation efforts began. Most species are divided, typically by environment, into populations with independent evolutionary trajectories. There are practical conservation objectives for defining these boundaries. Separate genetic clusters provide future evolutionary potential as environments change, and individuals in isolated populations may lose fitness when population size is reduced. The history of the effort to define units is briefly reviewed here, but I focus on finding a process that may facilitate uniform and effective application at a time when conservation urgency is great. I propose a refinement of the designated unit concept, distinguishing between conservation units (CUs) and evolutionarily sustaining conservation units (ESCUs).

Genomics reveals the role of admixture in the evolution of structure among sperm whale populations within the Mediterranean Sea.

In oceanic ecosystems, the nature of barriers to gene flow and the processes by which populations may become isolated are different from the terrestrial environment, and less well understood. In this study we investigate a highly mobile species (the sperm whale, Physeter macrocephalus) that is genetically differentiated between an open North Atlantic population and the populations in the Mediterranean Sea. We apply high-resolution single nucleotide polymorphism (SNP) analysis to study the nature of barriers to gene flow in this system, assessing the putative boundary into the Mediterranean (Strait of Gibraltar and Alboran Sea region), and including novel analyses on structuring among sperm whale populations within the Mediterranean basin. Our data support a recent founding of the Mediterranean population, around the time of the last glacial maximum, and show concerted historical demographic profiles in both the Atlantic and the Mediterranean. In each region there is evidence for a population decline around the time of the founder event. The largest decline was seen within the Mediterranean Sea where effective population size is substantially lower (especially in the eastern basin). While differentiation is strongest at the Atlantic/Mediterranean boundary, there is also weaker but significant differentiation between the eastern and western basins of the Mediterranean Sea. We propose, however, that the mechanisms are different. While post-founding gene flow was reduced between the Mediterranean and Atlantic populations, within the Mediterranean an important factor differentiating the basins is probably a greater degree of admixture between the western basin and the North Atlantic and some level of isolation between the western and eastern Mediterranean basins. Subdivision within the Mediterranean Sea exacerbates conservation concerns and will require consideration of what distinct impacts may affect populations in the two basins.

Museum specimens of a landlocked pinniped reveal recent loss of genetic diversity and unexpected population connections.

The Saimaa ringed seal (Pusa hispida saimensis) is endemic to Lake Saimaa in Finland. The subspecies is thought to have originated when parts of the ringed seal population of the Baltic region were trapped in lakes emerging due to postglacial bedrock rebound around 9000 years ago. During the 20th century, the population experienced a drastic human-induced bottleneck. Today encompassing a little over 400 seals with extremely low genetic diversity, it is classified as endangered. We sequenced sections of the mitochondrial control region from 60 up to 125-years-old museum specimens of the Saimaa ringed seal. The generated dataset was combined with publicly available sequences. We studied how genetic variation has changed through time in this subspecies and how it is phylogenetically related to other ringed seal populations from the Baltic Sea, Lake Ladoga, North America, Svalbard, and the White Sea. We observed temporal fluctuations in haplotype frequencies and loss of haplotypes accompanied by a recent reduction in female effective population size. In apparent contrast with the traditionally held view of the Baltic origin of the population, the Saimaa ringed seal mtDNA variation also shows affinities to North American ringed seals. Our results suggest that the Saimaa ringed seal has experienced recent genetic drift associated with small population size. The results further suggest that extant Baltic ringed seal is not representative of the ancestral population of the Saimaa ringed seal, which calls for re-evaluation of the deep history of this subspecies.

Strong and lasting impacts of past global warming on baleen whales and their prey.

Global warming is affecting the population dynamics and trophic interactions across a wide range of ecosystems and habitats. Translating these real-time effects into their long-term consequences remains a challenge. The rapid and extreme warming period that occurred after the Last Glacial Maximum (LGM) during the Pleistocene-Holocene transition (7-12 thousand years ago) provides an opportunity to gain insights into the long-term responses of natural populations to periods with global warming. The effects of this post-LGM warming period have been assessed in many terrestrial taxa, whereas insights into the impacts of rapid global warming on marine taxa remain limited, especially for megafauna. In order to understand how large-scale climate fluctuations during the post-LGM affected baleen whales and their prey, we conducted an extensive, large-scale analysis of the long-term effects of the post-LGM warming on abundance and inter-ocean connectivity in eight baleen whale and seven prey (fish and invertebrates) species across the Southern and the North Atlantic Ocean; two ocean basins that differ in key oceanographic features. The analysis was based upon 7032 mitochondrial DNA sequences as well as genome-wide DNA sequence variation in 100 individuals. The estimated temporal changes in genetic diversity during the last 30,000 years indicated that most baleen whale populations underwent post-LGM expansions in both ocean basins. The increase in baleen whale abundance during the Holocene was associated with simultaneous changes in their prey and climate. Highly correlated, synchronized and exponential increases in abundance in both baleen whales and their prey in the Southern Ocean were indicative of a dramatic increase in ocean productivity. In contrast, the demographic fluctuations observed in baleen whales and their prey in the North Atlantic Ocean were subtle, varying across taxa and time. Perhaps most important was the observation that the ocean-wide expansions and decreases in abundance that were initiated by the post-LGM global warming, continued for millennia after global temperatures stabilized, reflecting persistent, long-lasting impacts of global warming on marine fauna.

Comparative genomics provides insights into the aquatic adaptations of mammals.

The ancestors of marine mammals once roamed the land and independently committed to an aquatic lifestyle. These macroevolutionary transitions have intrigued scientists for centuries. Here, we generated high-quality genome assemblies of 17 marine mammals (11 cetaceans and six pinnipeds), including eight assemblies at the chromosome level. Incorporating previously published data, we reconstructed the marine mammal phylogeny and population histories and identified numerous idiosyncratic and convergent genomic variations that possibly contributed to the transition from land to water in marine mammal lineages. Genes associated with the formation of blubber (NFIA), vascular development (SEMA3E), and heat production by brown adipose tissue (UCP1) had unique changes that may contribute to marine mammal thermoregulation. We also observed many lineage-specific changes in the marine mammals, including genes associated with deep diving and navigation. Our study advances understanding of the timing, pattern, and molecular changes associated with the evolution of mammalian lineages adapting to aquatic life.

Population structure associated with bioregion and seasonal prey distribution for Indo-Pacific bottlenose dolphins (Tursiops aduncus) in South Africa.

Many marine species exhibit fine-scale population structure despite high mobility and a lack of physical barriers to dispersal, but the evolutionary drivers of differentiation in these systems are generally poorly understood. Here we investigate the potential role of habitat transitions and seasonal prey distributions on the evolution of population structure in the Indo-Pacific bottlenose dolphin, Tursiops aduncus, off South Africa's coast, using double-digest restriction-site associated DNA sequencing. Population structure was identified between the eastern and southern coasts and correlated with the habitat transition between the temperate Agulhas (southern) and subtropical Natal (eastern) Bioregions, suggesting differentiation driven by resource specializations. Differentiation along the Natal coast was comparatively weak, but was evident in some analyses and varied depending on whether the samples were collected during or outside the seasonal sardine (Sardinops sagax) run. This local abundance of prey could influence the ranging patterns and apparent genetic structure of T. aduncus. These findings have significant and transferable management implications, most importantly in terms of differentiating populations inhabiting distinct bioregions and seasonal structural patterns within a region associated with the movement of prey resources.

Natal origin of Namibian grey whale implies new distance record for in-water migration.

We use genomics to identify the natal origin of a grey whale found in the South Atlantic, at least 20 000 km from the species core range (halfway around the world). The data indicate an origin in the North Pacific, possibly from the endangered western North Pacific population, thought to include only approximately 200 individuals. This contributes to our understanding of Atlantic sightings of this species known primarily from the North Pacific, and could have conservation implications if grey whales have the potential for essentially global dispersion. More broadly, documenting and understanding rare extreme migration events have potential implications for the understanding of how a species may be able to respond to global change.

Genomic signatures of divergent selection are associated with social behaviour for spinner dolphin ecotypes.

Understanding the genomic basis of adaptation is critical for understanding evolutionary processes and predicting how species will respond to environmental change. Spinner dolphins in the eastern tropical Pacific (ETP) present a unique system for studying adaptation. Within this large geographical region are four spinner dolphin ecotypes with weak neutral genetic divergence and no obvious barriers to gene flow, but strong spatial variation in morphology, behaviour and habitat. These ecotypes have large population sizes, which could reduce the effects of drift and facilitate selection. To identify genomic regions putatively under divergent selective pressures between ecotypes, we used genome scans with 8994 RADseq single nucleotide polymorphisms (SNPs) to identify population differentiation outliers and genotype-environment association outliers. Gene ontology enrichment analyses indicated that outlier SNPs from both types of analyses were associated with multiple genes involved in social behaviour and hippocampus development, including 15 genes associated with the human social disorder autism. Evidence for divergent selection on social behaviour is supported by previous evidence that these spinner dolphin ecotypes differ in mating systems and associated social behaviours. In particular, three of the ETP ecotypes probably have a polygynous mating system characterized by strong premating competition among males, whereas the fourth ecotype probably has a polygynandrous mating system characterized by strong postmating competition such as sperm competition. Our results provide evidence that selection for social behaviour may be an evolutionary force driving diversification of spinner dolphins in the ETP, potentially as a result of divergent sexual selection associated with different mating systems. Future studies should further investigate the potential adaptive role of the candidate genes identified here, and could probably find further signatures of selection using whole genome sequence data.

Detecting genetic signals of selection in heavily bottlenecked reindeer populations by comparing parallel founder events.

Founder populations are of special interest to both evolutionary and conservation biologists, but the detection of genetic signals of selection in these populations is challenging due to their demographic history. Geographically separated founder populations likely to have been subjected to similar selection pressures provide an ideal but rare opportunity to overcome these challenges. Here we take advantage of such a situation generated when small, isolated founder populations of reindeer were established on the island of South Georgia, and using this system we look for empirical evidence of selection overcoming strong genetic drift. We generated a 70 k ddRADseq single nucleotide polymorphism database for the two parallel reindeer founder populations and screened for signatures of soft sweeps. We find evidence for a genomic region under selection shared among the two populations, and support our findings with Wright-Fisher model simulations to assess the power and specificity of interpopulation selection scans-namely Bayescan, OutFLANK, PCadapt and a newly developed scan called Genome Wide Differentiation Scan (GWDS)-in the context of pairwise source-founder comparisons. Our simulations indicate that loci under selection in small founder populations are most probably detected by GWDS, and strengthen the hypothesis that the outlier region represents a true locus under selection. We explore possible, relevant functional roles for genes in linkage with the detected outlier loci.

SambaR: An R package for fast, easy and reproducible population-genetic analyses of biallelic SNP data sets.

SNP data sets can be used to infer a wealth of information about natural populations, including information about their structure, genetic diversity, and the presence of loci under selection. However, SNP data analysis can be a time-consuming and challenging process, not in the least because at present many different software packages are needed to execute and depict the wide variety of mainstream population-genetic analyses. Here, we present SambaR, an integrative and user-friendly R package which automates and simplifies quality control and population-genetic analyses of biallelic SNP data sets. SambaR allows users to perform mainstream population-genetic analyses and to generate a wide variety of ready to publish graphs with a minimum number of commands (less than 10). These wrapper commands call functions of existing packages (including adegenet, ape, LEA, poppr, pcadapt and StAMPP) as well as new tools uniquely implemented in SambaR. We tested SambaR on online available SNP data sets and found that SambaR can process data sets of over 100,000 SNPs and hundreds of individuals within hours, given sufficient computing power. Newly developed tools implemented in SambaR facilitate optimization of filter settings, objective interpretation of ordination analyses, enhance comparability of diversity estimates from reduced representation library SNP data sets, and generate reduced SNP panels and structure-like plots with Bayesian population assignment probabilities. SambaR facilitates rapid population genetic analyses on biallelic SNP data sets by removing three major time sinks: file handling, software learning, and data plotting. In addition, SambaR provides a convenient platform for SNP data storage and management, as well as several new utilities, including guidance in setting appropriate data filters. The SambaR source script, manual and example data set are distributed through GitHub: https://github.com/mennodejong1986/SambaR.

Demography and adaptation promoting evolutionary transitions in a mammalian genus that diversified during the Pleistocene.

Species that evolved in temperate regions during the Pleistocene experienced periods of extreme climatic transitions. Consequent population fragmentation and dynamics had the potential to generate small, isolated populations where the influence of genetic drift would be expected to be strong. We use comparative genomics to assess the evolutionary influence of historical demographics and natural selection through a series of transitions associated with the formation of the genus Capreolus, speciation within this genus during the Quaternary and during divergence among European roe deer (C. capreolus) populations. Our analyses were facilitated by the generation of a new high-coverage reference genome for the Siberian roe deer (C. pygargus). We find progressive reductions in effective population size (Ne ), despite very large census sizes in modern C. capreolus populations and show that low Ne has impacted the C. capreolus genome, reducing diversity and increasing linkage disequilibrium. Even so, we find evidence for natural selection shared among C. capreolus populations, including a historically documented founder population that has been through a severe bottleneck. During each phylogenetic transition there is evidence for selection (from dN/dS and nucleotide diversity tests), including at loci associated with diapause (delayed embryonic development), a phenotype restricted to this genus among the even-toed ungulates. Together these data allow us to assess expectations for the origin and diversification of a mammalian genus during a period of extreme environmental change.

Sex-specific impact of inbreeding on pathogen load in the striped dolphin.

The impact of inbreeding on fitness has been widely studied and provides consequential inference about adaptive potential and the impact on survival for reduced and fragmented natural populations. Correlations between heterozygosity and fitness are common in the literature, but they rarely inform about the likely mechanisms. Here, we investigate a pathology with a clear impact on health in striped dolphin hosts (a nematode infection that compromises lung function). Dolphins varied with respect to their parasite burden of this highly pathogenic lung nematode (Skrjabinalius guevarai). Genetic diversity revealed by high-resolution restriction-associated DNA (43 018 RADseq single nucleotide polymorphisms) analyses showed a clear association between heterozygosity and pathogen load, but only for female dolphins, for which the more heterozygous individuals had lower Sk. guevarai burden. One locus identified by RADseq was a strong outlier in association with parasite load (heterozygous in all uninfected females, homozygous for 94% of infected females), found in an intron of the citron rho-interacting serine/threonine kinase locus (associated with milk production in mammals). Allelic variation at the Class II major histocompatability complex DQB locus was also assessed and found to be associated with both regional variation and with pathogen load. Both sex specificity and the identification of associating functional loci provide insight into the mechanisms by which more inbred individuals may be more susceptible to the infection of this parasite. This provides important insight towards our understanding of the impact of inbreeding in natural populations, relevant to both evolutionary and practical conservation considerations.

Phylogenomics of the genus Tursiops and closely related Delphininae reveals extensive reticulation among lineages and provides inference about eco-evolutionary drivers.

Phylogeographic inference has provided extensive insight into the relative roles of geographical isolation and ecological processes during evolutionary radiations. However, the importance of cross-lineage admixture in facilitating adaptive radiations is increasingly being recognised, and suggested as a main cause of phylogenetic uncertainty. In this study, we used a double digest RADseq protocol to provide a high resolution (~4 Million bp) nuclear phylogeny of the Delphininae. Phylogenetic resolution of this group has been especially intractable, likely because it has experienced a recent species radiation. We carried out cross-lineage reticulation analyses, and tested for several sources of potential bias in determining phylogenies from genome sampling data. We assessed the divergence time and historical demography of T. truncatus and T. aduncus by sequencing the T. aduncus genome and comparing it with the T. truncatus reference genome. Our results suggest monophyly for the genus Tursiops, with the recently proposed T. australis species falling within the T. aduncus lineage. We also show the presence of extensive cross-lineage gene flow between pelagic and European coastal ecotypes of T. truncatus, as well as in the early stages of diversification between spotted (Stenella frontalis; Stenella attenuata), spinner (Stenella longirostris), striped (Stenella coeruleoalba), common (Delphinus delphis), and Fraser's (Lagenodelphis hosei) dolphins. Our study suggests that cross-lineage gene flow in this group has been more extensive and complex than previously thought. In the context of biogeography and local habitat dependence, these results improve our understanding of the evolutionary processes determining the history of this lineage.