Multinational evaluation of genetic diversity indicators for the Kunming-Montreal Global Biodiversity Framework.

Under the recently adopted Kunming-Montreal Global Biodiversity Framework, 196 Parties committed to reporting the status of genetic diversity for all species. To facilitate reporting, three genetic diversity indicators were developed, two of which focus on processes contributing to genetic diversity conservation: maintaining genetically distinct populations and ensuring populations are large enough to maintain genetic diversity. The major advantage of these indicators is that they can be estimated with or without DNA-based data. However, demonstrating their feasibility requires addressing the methodological challenges of using data gathered from diverse sources, across diverse taxonomic groups, and for countries of varying socio-economic status and biodiversity levels. Here, we assess the genetic indicators for 919 taxa, representing 5271 populations across nine countries, including megadiverse countries and developing economies. Eighty-three percent of the taxa assessed had data available to calculate at least one indicator. Our results show that although the majority of species maintain most populations, 58% of species have populations too small to maintain genetic diversity. Moreover, genetic indicator values suggest that IUCN Red List status and other initiatives fail to assess genetic status, highlighting the critical importance of genetic indicators.

Limited historical admixture between European wildcats and domestic cats.

Domestic cats were derived from the Near Eastern wildcat (Felis lybica), after which they dispersed with people into Europe. As they did so, it is possible that they interbred with the indigenous population of European wildcats (Felis silvestris). Gene flow between incoming domestic animals and closely related indigenous wild species has been previously demonstrated in other taxa, including pigs, sheep, goats, bees, chickens, and cattle. In the case of cats, a lack of nuclear, genome-wide data, particularly from Near Eastern wildcats, has made it difficult to either detect or quantify this possibility. To address these issues, we generated 75 ancient mitochondrial genomes, 14 ancient nuclear genomes, and 31 modern nuclear genomes from European and Near Eastern wildcats. Our results demonstrate that despite cohabitating for at least 2,000 years on the European mainland and in Britain, most modern domestic cats possessed less than 10% of their ancestry from European wildcats, and ancient European wildcats possessed little to no ancestry from domestic cats. The antiquity and strength of this reproductive isolation between introduced domestic cats and local wildcats was likely the result of behavioral and ecological differences. Intriguingly, this long-lasting reproductive isolation is currently being eroded in parts of the species' distribution as a result of anthropogenic activities.

Genetic swamping of the critically endangered Scottish wildcat was recent and accelerated by disease.

The European wildcat population in Scotland is considered critically endangered as a result of hybridization with introduced domestic cats,1,2 though the time frame over which this gene flow has taken place is unknown. Here, using genome data from modern, museum, and ancient samples, we reconstructed the trajectory and dated the decline of the local wildcat population from viable to severely hybridized. We demonstrate that although domestic cats have been present in Britain for over 2,000 years,3 the onset of hybridization was only within the last 70 years. Our analyses reveal that the domestic ancestry present in modern wildcats is markedly over-represented in many parts of the genome, including the major histocompatibility complex (MHC). We hypothesize that introgression provides wildcats with protection against diseases harbored and introduced by domestic cats, and that this selection contributes to maladaptive genetic swamping through linkage drag. Using the case of the Scottish wildcat, we demonstrate the importance of local ancestry estimates to both understand the impacts of hybridization in wild populations and support conservation efforts to mitigate the consequences of anthropogenic and environmental change.

Historic Sampling of a Vanishing Beast: Population Structure and Diversity in the Black Rhinoceros.

The black rhinoceros (Diceros bicornis L.) is a critically endangered species historically distributed across sub-Saharan Africa. Hunting and habitat disturbance have diminished both its numbers and distribution since the 19th century, but a poaching crisis in the late 20th century drove them to the brink of extinction. Genetic and genomic assessments can greatly increase our knowledge of the species and inform management strategies. However, when a species has been severely reduced, with the extirpation and artificial admixture of several populations, it is extremely challenging to obtain an accurate understanding of historic population structure and evolutionary history from extant samples. Therefore, we generated and analyzed whole genomes from 63 black rhinoceros museum specimens collected between 1775 and 1981. Results showed that the black rhinoceros could be genetically structured into six major historic populations (Central Africa, East Africa, Northwestern Africa, Northeastern Africa, Ruvuma, and Southern Africa) within which were nested four further subpopulations (Maasailand, southwestern, eastern rift, and northern rift), largely mirroring geography, with a punctuated north-south cline. However, we detected varying degrees of admixture among groups and found that several geographical barriers, most prominently the Zambezi River, drove population discontinuities. Genomic diversity was high in the middle of the range and decayed toward the periphery. This comprehensive historic portrait also allowed us to ascertain the ancestry of 20 resequenced genomes from extant populations. Lastly, using insights gained from this unique temporal data set, we suggest management strategies, some of which require urgent implementation, for the conservation of the remaining black rhinoceros diversity.

The Contribution of Digital Sequence Information to Conservation Biology: A Southern African Perspective.

Many recent contributions have made a compelling case that genetic diversity is not adequately reflected in international frameworks and policies, as well as in local governmental processes implementing such frameworks. Using digital sequence information (DSI) and other publicly available data is supported to assess genetic diversity, toward formulation of practical actions for long-term conservation of biodiversity, with the particular goal of maintaining ecological and evolutionary processes. Given the inclusion of specific goals and targets regarding DSI in the latest draft of the Global Biodiversity Framework negotiated at the 15th Conference of the Parties (COP15) in Montreal in December 2022 and the crucial decisions on access and benefit sharing to DSI that will be taken in the coming months and future COP meetings, a southern African perspective on how and why open access to DSI is essential for the conservation of intraspecific biodiversity (genetic diversity and structure) across country borders is provided.

The microscopic five of the big five: Managing zoonotic diseases within and beyond African wildlife protected areas.

African protected areas strive to conserve the continent's great biodiversity with a targeted focus on the flagship 'Big Five' megafauna. Though often not considered, this biodiversity protection also extends to the lesser-known microbes and parasites that are maintained in these diverse ecosystems, often in a silent and endemically stable state. Climate and anthropogenic change, and associated diversity loss, however, are altering these dynamics leading to shifts in ecological interactions and pathogen spill over into new niches and hosts. As many African protected areas are bordered by game and livestock farms, as well as villages, they provide an ideal study system to assess infection dynamics at the human-livestock-wildlife interface. Here we review five zoonotic, multi-host diseases (bovine tuberculosis, brucellosis, Rift Valley fever, schistosomiasis and cryptosporidiosis)-the 'Microscopic Five'-and discuss the biotic and abiotic drivers of parasite transmission using the iconic Kruger National Park, South Africa, as a case study. We identify knowledge gaps regarding the impact of the 'Microscopic Five' on wildlife within parks and highlight the need for more empirical data, particularly for neglected (schistosomiasis) and newly emerging (cryptosporidiosis) diseases, as well as zoonotic disease risk from the rising bush meat trade and game farm industry. As protected areas strive to become further embedded in the socio-economic systems that surround them, providing benefits to local communities, One Health approaches can help maintain the ecological integrity of ecosystems, while protecting local communities and economies from the negative impacts of disease.

Species Separation within, and Preliminary Phylogeny for, the Leafhopper Genus Anoscopus with Particular Reference to the Putative British Endemic Anoscopus duffieldi (Hemiptera: Cicadellidae).

The subfamily Aphrodinae (Hemiptera: Cicadellidae) contains ~33 species in Europe within four genera. Species in two genera in particular, Aphrodes and Anoscopus, have proved to be difficult to distinguish morphologically. Our aim was to determine the status of the putative species Anoscopus duffieldi, found only on the RSPB Nature Reserve at Dungeness, Kent, a possible rare UK endemic. DNA from samples of all seven UK Anoscopus species (plus Anoscopusalpinus from the Czech Republic) were sequenced using parts of the mitochondrial cytochrome oxidase I and 16S rRNA genes. Bayesian inference phylogenies were created. Specimens of each species clustered into monophyletic groups, except for Anoscopusalbifrons, A. duffieldi and Anoscopuslimicola. Two A. albifrons specimens grouped with A. duffieldi repeatedly with strong support, and the remaining A. albifrons clustered within A. limicola. Genetic distances suggest that A. albifrons and A. limicola are a single interbreeding population (0% divergence), while A. albifrons and A. duffieldi diverged by only 0.28%. Shared haplotypes between A. albifrons, A. limicola and A. duffieldi strongly suggest interbreeding, although misidentification may also explain these topologies. However, all A. duffieldi clustered together in the trees. A conservative approach might be to treat A. duffieldi, until other evidence is forthcoming, as a possible endemic subspecies.

Interspecific Gene Flow and the Evolution of Specialization in Black and White Rhinoceros.

Africa's black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros are closely related sister-taxa that evolved highly divergent obligate browsing and grazing feeding strategies. Although their precursor species Diceros praecox and Ceratotherium mauritanicum appear in the fossil record ∼5.2 Ma, by 4 Ma both were still mixed feeders, and were even spatiotemporally sympatric at several Pliocene sites in what is today Africa's Rift Valley. Here, we ask whether or not D. praecox and C. mauritanicum were reproductively isolated when they came into Pliocene secondary contact. We sequenced and de novo assembled the first annotated black rhinoceros reference genome and compared it with available genomes of other black and white rhinoceros. We show that ancestral gene flow between D. praecox and C. mauritanicum ceased sometime between 3.3 and 4.1 Ma, despite conventional methods for the detection of gene flow from whole genome data returning false positive signatures of recent interspecific migration due to incomplete lineage sorting. We propose that ongoing Pliocene genetic exchange, for up to 2 My after initial divergence, could have potentially hindered the development of obligate feeding strategies until both species were fully reproductively isolated, but that the more severe and shifting paleoclimate of the early Pleistocene was likely the ultimate driver of ecological specialization in African rhinoceros.

Dispersal and genetic structure in a tropical small mammal, the Bornean tree shrew (Tupaia longipes), in a fragmented landscape along the Kinabatangan River, Sabah, Malaysia.

BACKGROUND: Constraints in migratory capabilities, such as the disruption of gene flow and genetic connectivity caused by habitat fragmentation, are known to affect genetic diversity and the long-term persistence of populations. Although negative population trends due to ongoing forest loss are widespread, the consequence of habitat fragmentation on genetic diversity, gene flow and genetic structure has rarely been investigated in Bornean small mammals. To fill this gap in knowledge, we used nuclear and mitochondrial DNA markers to assess genetic diversity, gene flow and the genetic structure in the Bornean tree shrew, Tupaia longipes, that inhabits forest fragments of the Lower Kinabatangan Wildlife Sanctuary, Sabah. Furthermore, we used these markers to assess dispersal regimes in male and female T. longipes. RESULTS: In addition to the Kinabatangan River, a known barrier for dispersal in tree shrews, the heterogeneous landscape along the riverbanks affected the genetic structure in this species. Specifically, while in larger connected forest fragments along the northern riverbank genetic connectivity was relatively undisturbed, patterns of genetic differentiation and the distribution of mitochondrial haplotypes in a local scale indicated reduced migration on the strongly fragmented southern riverside. Especially, oil palm plantations seem to negatively affect dispersal in T. longipes. Clear sex-biased dispersal was not detected based on relatedness, assignment tests, and haplotype diversity. CONCLUSION: This study revealed the importance of landscape connectivity to maintain migration and gene flow between fragmented populations, and to ensure the long-term persistence of species in anthropogenically disturbed landscapes.

Inferring fine-scale spatial structure of the brown bear (Ursus arctos) population in the Carpathians prior to infrastructure development.

Landscape genetics is increasingly being used in landscape planning for biodiversity conservation by assessing habitat connectivity and identifying landscape barriers, using intraspecific genetic data and quantification of landscape heterogeneity to statistically test the link between genetic variation and landscape variability. In this study we used genetic data to understand how landscape features and environmental factors influence demographic connectedness in Europe's largest brown bear population and to assist in mitigating planned infrastructure development in Romania. Model-based clustering inferred one large and continuous bear population across the Carpathians suggesting that suitable bear habitat has not become sufficiently fragmented to restrict movement of individuals. However, at a finer scale, large rivers, often located alongside large roads with heavy traffic, were found to restrict gene flow significantly, while eastern facing slopes promoted genetic exchange. Since the proposed highway infrastructure development threatens to fragment regions of the Carpathians where brown bears occur, we develop a decision support tool based on models that assess the landscape configuration needed for brown bear conservation using wildlife corridor parameters. Critical brown bear corridors were identified through spatial mapping and connectivity models, which may be negatively influenced by infrastructure development and which therefore require mitigation. We recommend that current and proposed infrastructure developments incorporate these findings into their design and where possible avoid construction measures that may further fragment Romania's brown bear population or include mitigation measures where alternative routes are not feasible.

Genomic selection strategies for breeding adaptation and production in dairy cattle under climate change.

Livestock production both contributes to and is affected by global climate change, and substantial modifications will be required to increase its climate resilience. In this context, reliance on dominant commercial livestock breeds, featuring small effective population sizes, makes current production strategies vulnerable if their production is restricted to environments, which may be too costly to support under future climate scenarios. The adaptability of animal populations to future environments will therefore become important. To help evaluate the role of genetics in climate adaptation, we compared selection strategies in dairy cattle using breeding simulations, where genomic selection was used on two negatively correlated traits for production (assumed to be moderately heritable) and adaptation (assumed to have low heritability). Compared with within-population breeding, genomic introgression produced a more positive genetic change for both production and adaptation traits. Genomic introgression from highly adapted but low production value populations into highly productive but low adaptation populations was most successful when the adaptation trait was given a lower selection weight than the production trait. Genomic introgression from highly productive population to highly adapted population was most successful when the adaptation trait was given a higher selection weight than the production trait. Both these genomic introgression schemes had the lowest risk of inbreeding. Our results suggest that both adaptation and production can potentially be improved simultaneously by genomic introgression.

Contrasting evolutionary history, anthropogenic declines and genetic contact in the northern and southern white rhinoceros (Ceratotherium simum).

The white rhinoceros (Ceratotherium simum) has a discontinuous African distribution, which is limited by the extent of sub-Saharan grasslands. The southern population (SWR) declined to its lowest number around the turn of the nineteenth century, but recovered to become the world's most numerous rhinoceros. In contrast, the northern population (NWR) was common during much of the twentieth century, declining rapidly since the 1970s, and now only two post-reproductive individuals remain. Despite this species's conservation status, it lacks a genetic assessment of its demographic history. We therefore sampled 232 individuals from extant and museum sources and analysed ten microsatellite loci and the mtDNA control region. Both marker types reliably partitioned the species into SWR and NWR, with moderate nuclear genetic diversity and only three mtDNA haplotypes for the species, including historical samples. We detected ancient interglacial demographic declines in both populations. Both populations may also have been affected by recent declines associated with the colonial expansion for the SWR, and with the much earlier Bantu migrations for the NWR. Finally, we detected post-divergence secondary contact between NWR and SWR, possibly occurring as recently as the last glacial maximum. These results suggest the species was subjected to regular periods of fragmentation and low genetic diversity, which may have been replenished upon secondary contact during glacial periods. The species's current situation thus reflects prehistoric declines that were exacerbated by anthropogenic pressure associated with the rise of late Holocene technological advancement in Africa. Importantly, secondary contact suggests a potentially positive outcome for a hybrid rescue conservation strategy, although further genome-wide data are desirable to corroborate these results.

Walking in a heterogeneous landscape: Dispersal, gene flow and conservation implications for the giant panda in the Qinling Mountains.

Understanding the interaction between life history, demography and population genetics in threatened species is critical for the conservations of viable populations. In the context of habitat loss and fragmentation, identifying the factors that underpin the structuring of genetic variation within populations can allow conservationists to evaluate habitat quality and connectivity and help to design dispersal corridors effectively. In this study, we carried out a detailed, fine-scale landscape genetic investigation of a giant panda population from the Qinling Mountains for the first time. With a large microsatellite data set and complementary analysis methods, we examined the role of isolation-by-barriers (IBB), isolation-by-distance (IBD) and isolation-by-resistance (IBR) in shaping the pattern of genetic variation in this giant panda population. We found that the Qinling population comprises one continuous genetic cluster, and among the landscape hypotheses tested, gene flow was found to be correlated with resistance gradients for two topographic factors, slope aspect and topographic complexity, rather than geographical distance or barriers. Gene flow was inferred to be facilitated by easterly slope aspect and to be constrained by topographically complex landscapes. These factors are related to benign microclimatic conditions for both the pandas and the food resources they rely on and more accessible topographic conditions for movement, respectively. We identified optimal corridors based on these results, aiming to promote gene flow between human-induced habitat fragments. These findings provide insight into the permeability and affinities of giant panda habitats and offer important reference for the conservation of the giant panda and its habitat.

Odour dialects among wild mammals.

Across multiple taxa, population structure and dynamics depend on effective signalling between individuals. Among mammals, chemical communication is arguably the most important sense, underpinning mate choice, parental care, territoriality and even disease transmission. There is a growing body of evidence that odours signal genetic information that may confer considerable benefits including inbreeding avoidance and nepotism. To date, however, there has been no clear evidence that odours encode population-level information in wild mammals. Here we demonstrate for the first time the existence of 'odour dialects' in genetically distinct mammalian subpopulations across a large geographical scale. We found that otters, Lutra lutra, from across the United Kingdom possess sex and biogeography-specific odours. Subpopulations with the most distinctive odour profiles are also the most genetically diverse but not the most genetically differentiated. Furthermore, geographic distance between individuals does not explain regional odour differences, refuting other potential explanations such as group odour sharing behaviour. Differences in the language of odours between subpopulations have the potential to affect individual interactions, which could impact reproduction and gene-flow.

Extinctions, genetic erosion and conservation options for the black rhinoceros (Diceros bicornis).

The black rhinoceros is again on the verge of extinction due to unsustainable poaching in its native range. Despite a wide historic distribution, the black rhinoceros was traditionally thought of as depauperate in genetic variation, and with very little known about its evolutionary history. This knowledge gap has hampered conservation efforts because hunting has dramatically reduced the species' once continuous distribution, leaving five surviving gene pools of unknown genetic affinity. Here we examined the range-wide genetic structure of historic and modern populations using the largest and most geographically representative sample of black rhinoceroses ever assembled. Using both mitochondrial and nuclear datasets, we described a staggering loss of 69% of the species' mitochondrial genetic variation, including the most ancestral lineages that are now absent from modern populations. Genetically unique populations in countries such as Nigeria, Cameroon, Chad, Eritrea, Ethiopia, Somalia, Mozambique, Malawi and Angola no longer exist. We found that the historic range of the West African subspecies (D. b. longipes), declared extinct in 2011, extends into southern Kenya, where a handful of individuals survive in the Masai Mara. We also identify conservation units that will help maintain evolutionary potential. Our results suggest a complete re-evaluation of current conservation management paradigms for the black rhinoceros.

Quantitative evaluation of hybridization and the impact on biodiversity conservation.

Anthropogenic hybridization is an increasing conservation threat worldwide. In South Africa, recent hybridization is threatening numerous ungulate taxa. For example, the genetic integrity of the near-threatened bontebok (Damaliscus pygargus pygargus) is threatened by hybridization with the more common blesbok (D. p. phillipsi). Identifying nonadmixed parental and admixed individuals is challenging based on the morphological traits alone; however, molecular analyses may allow for accurate detection. Once hybrids are identified, population simulation software may assist in determining the optimal conservation management strategy, although quantitative evaluation of hybrid management is rarely performed. In this study, our objectives were to describe species-wide and localized rates of hybridization in nearly 3,000 individuals based on 12 microsatellite loci, quantify the accuracy of hybrid assignment software (STRUCTURE and NEWHYBRIDS), and determine an optimal threshold of bontebok ancestry for management purposes. According to multiple methods, we identified 2,051 bontebok, 657 hybrids, and 29 blesbok. More than two-thirds of locations contained at least some hybrid individuals, with populations varying in the degree of introgression. HYBRIDLAB was used to simulate four generations of coexistence between bontebok and blesbok, and to optimize a threshold of ancestry, where most hybrids will be detected and removed, and the fewest nonadmixed bontebok individuals misclassified as hybrids. Overall, a threshold Q-value (admixture coefficient) of 0.90 would remove 94% of hybrid animals, while a threshold of 0.95 would remove 98% of hybrid animals but also 8% of nonadmixed bontebok. To this end, a threshold of 0.90 was identified as optimal and has since been implemented in formal policy by a provincial nature conservation agency. Due to widespread hybridization, effective conservation plans should be established and enforced to conserve native populations that are genetically unique.

Landscape determinants of fine-scale genetic structure of a small rodent in a heterogeneous landscape (Hluhluwe-iMfolozi Park, South Africa).

Small mammals provide ecosystem services, acting, for example, as pollinators and seed dispersers. In addition, they are also disease reservoirs that can be detrimental to human health and they can also act as crop pests. Knowledge of their dispersal preferences is therefore useful for population management and landscape planning. Genetic data were used alongside landscape data to examine the influence of the landscape on the demographic connectedness of the Natal multimammate mouse (Mastomys natalensis) and to identify landscape characteristics that influence the genetic structure of this species across a spatially and temporally varying environment. The most significant landscape features shaping gene flow were aspect, vegetation cover, topographic complexity (TC) and rivers, with western facing slopes, topographic complexity and rivers restricting gene flow. In general, thicket vegetation was correlated with increased gene flow. Identifying features of the landscape that facilitate movement/dispersal in M. natalensis potentially has application for other small mammals in similar ecosystems. As the primary reservoir host of the zoonotic Lassa virus, a landscape genetics approach may have applications in determining areas of high disease risk to humans. Identifying these landscape features may also be important in crop management due to damage by rodent pests.

Bioregion heterogeneity correlates with extensive mitochondrial DNA diversity in the Namaqua rock mouse, Micaelamys namaquensis (Rodentia: Muridae) from southern Africa--evidence for a species complex.

BACKGROUND: Intraspecific variation within the diverse southern African murine rodents has not been extensively investigated, yet cryptic diversity is evident in several taxa studied to date. The Namaqua rock mouse, Micaelamys namaquensis Smith, 1834 is a widespread endemic murine rodent from the subregion. Currently, a single species with four subspecies is recognised, but in the past up to 16 subspecies were described. Thus, this species is a good candidate for the investigation of patterns and processes of diversification in a diverse but under-studied mammalian subfamily and geographic region. Here, we report genetic differentiation based on mitochondrial DNA (mtDNA) cytochrome b (cyt b) sequences among samples collected over an extensive coverage of the species' range. RESULTS: Cytochrome b sequences of 360 widely sampled individuals identified 137 unique maternal alleles. Gene tree and phylogeographic analyses of these alleles suggest the presence of at least eight lineages or haplogroups (A-H), with varying degrees of intra-lineage diversity. This differentiation is in contrast with the most recent taxonomic treatment based on cranial morphometrics which only recognised four subspecies. The mtDNA diversity strongly supports earlier views that this taxon may represent a species complex. We further show statistical support for the association of several of these lineages with particular vegetation biomes of southern Africa. The time to the most recent common ancestor (TMRCA) dates to the Pliocene (~5 Mya) whereas coalescent-based divergence time estimates between lineages vary between 813 Kya [0.22-1.36] and 4.06 Mya [1.21-4.47]. The major diversification within lineages occurred during the Pleistocene. The identification of several regions of sympatry of distinct lineages offers future opportunities for the elucidation of the underlying speciation processes in the suggested species complex. CONCLUSIONS: Similar to other African murine rodents, M. namaquensis radiated during the Pliocene and Pleistocene coinciding with major periods of aridification and the expansion of savanna habitats. The suggested species complex is represented by at least eight lineages of which the majority are confined to only one or a few neighbouring biomes/bioregions. Contrasting intra-lineage phylogeographic patterns suggest differences in adaptation and responses to Plio-Pleistocene climatic and vegetation changes. The role of ecological factors in driving speciation in the group needs further investigation.