Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population

The process and consequences of hybridization are of interest to evolutionary biologists because of the importance of hybridization in understanding reproductive isolation, speciation, and the influence of introgression on population genetic structure. Recent studies of hybridization have been enhanced by the advent of sensitive, genetic marker-based techniques for inferring the degree of admixture occurring within individuals. Here we present a genetic marker-based analysis of hybridization in a large-bodied, long-lived mammal over multiple generations. We analysed patterns of hybridization between yellow baboons (Papio cynocephalus) and anubis baboons (Papio anubis) in a well-studied natural population in Amboseli National Park, Kenya, using genetic samples from 450 individuals born over the last 36 years. We assigned genetic hybrid scores based on genotypes at 14 microsatellite loci using the clustering algorithm implemented in STRUCTURE 2.0, and assessed the robustness of these scores by comparison to pedigree information and through simulation. The genetic hybrid scores showed generally good agreement with previous morphological assessments of hybridity, but suggest that genetic methods may be more sensitive for identification of low levels of hybridity. The results of our analysis indicate that the proportion of hybrids in the Amboseli population has grown over time, but that the average proportion of anubis ancestry within hybrids is gradually decreasing. We argue that these patterns are probably a result of both selective and nonselective processes, including differences in the timing of life-history events for hybrid males relative to yellow baboon males, and stochasticity in long-distance dispersal from the source anubis population into Amboseli.     

Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli, Kenya

In 1986, Samuels and Altmann reported evidence for a hybrid zone between Papio anubis and Papio cynocephalus in Amboseli, Kenya, in a baboon population that has been the subject of long-term study since 1971 [Samuels & Altmann, International Journal of Primatology 7:131-138, 1986]. In the current report we document ongoing patterns of hybridization in Amboseli between anubis and yellow baboons. In July 2000, we exhaustively scored living members of study groups for their degree of hybridity, using seven phenotypic characteristics (five in juveniles). We also scored all former members of study groups on the basis of photographic records, field notes, and observer recollections. A total of five anubis males and 11 males with hybrid phenotypes have immigrated into study groups over the course of the long-term study, and immigrations by hybrid males have increased in frequency over time. Further, the increasing frequency of hybrid phenotypes among animals born into study groups indicates that anubis and hybrid males have successfully reproduced in study groups. However, hybrid phenotypes and anubis immigrations were limited to groups in the southwestern portion of the Amboseli basin, with no hybrids occurring in the six eastern groups. Finally, we present evidence that anubis and hybrid males in Amboseli exhibit patterns of natal dispersal that are different from those of yellow males in Amboseli: males with anubis or hybrid phenotypes were significantly more likely to immigrate as juveniles or young subadults than were yellow males.     

Genomewide ancestry and divergence patterns from low‐coverage sequencing data reveal a complex history of admixture in wild baboons

Naturally occurring admixture has now been documented in every major primate lineage, suggesting its key role in primate evolutionary history. Active primate hybrid zones can provide valuable insight into this process. Here, we investigate the history of admixture in one of the best‐studied natural primate hybrid zones, between yellow baboons (Papio cynocephalus) and anubis baboons (Papio anubis) in the Amboseli ecosystem of Kenya. We generated a new genome assembly for yellow baboon and low‐coverage genomewide resequencing data from yellow baboons, anubis baboons and known hybrids (n = 44). Using a novel composite likelihood method for estimating local ancestry from low‐coverage data, we found high levels of genetic diversity and genetic differentiation between the parent taxa, and excellent agreement between genome‐scale ancestry estimates and a priori pedigree, life history and morphology‐based estimates (r² = 0.899). However, even putatively unadmixed Amboseli yellow individuals carried a substantial proportion of anubis ancestry, presumably due to historical admixture. Further, the distribution of shared vs. fixed differences between a putatively unadmixed Amboseli yellow baboon and an unadmixed anubis baboon, both sequenced at high coverage, is inconsistent with simple isolation–migration or equilibrium migration models. Our findings suggest a complex process of intermittent contact that has occurred multiple times in baboon evolutionary history, despite no obvious fitness costs to hybrids or major geographic or behavioural barriers. In combination with the extensive phenotypic data available for baboon hybrids, our results provide valuable context for understanding the history of admixture in primates, including in our own lineage.     

Age at maturity in wild baboons: genetic, environmental and demographic influences

The timing of early life-history events, such as sexual maturation and first reproduction, can greatly influence variation in individual fitness. In this study, we analysed possible sources of variation underlying different measures of age at social and physical maturation in wild baboons in the Amboseli basin, Kenya. The Amboseli baboons are a natural population primarily comprised of yellow baboons (Papio cynocephalus) that occasionally hybridize with anubis baboons (Papio anubis) from outside the basin. We found that males and females differed in the extent to which various factors influenced their maturation. Surprisingly, we found that male maturation was most strongly related to the proportion of anubis ancestry revealed by their microsatellite genotypes: hybrid males matured earlier than yellow males. In contrast, although hybrid females reached menarche slightly earlier than yellow females, maternal rank and the presence of maternal relatives had the largest effects on female maturation, followed by more modest effects of group size and rainfall. Our results indicate that a complex combination of demographic, genetic, environmental, and maternal effects contribute to variation in the timing of these life-history milestones.     

Immigration of aPapio anubis male into a group ofPapio cynocephalus baboons and

The 1982 observation of the immigration of an adult male olive baboon, Papio anubis,into a group of yellow baboons, Papio cynocephalus,in Amboseli National Park, Kenya, constitutes the first confirmed report of interbreeding between the two species within the Amboseli baboon population. We document the social aspects of the immigration and describe subsequent sightings of anubisbaboons in Amboseli that confirm the existence of a previously unrecognized hybrid zone in Kenya.     

Ecology and age,but not genetic ancestry,predict fetal loss in a wild baboon hybrid zone

Objectives

Pregnancy failure represents a major fitness cost for any mammal, particularly those with slow life histories such as primates. Here, we quantified the risk of fetal loss in wild hybrid baboons, including genetic, ecological, and demographic sources of variance. We were particularly interested in testing the hypothesis that hybridization increases fetal loss rates. Such an effect would help explain how baboons may maintain genetic and phenotypic integrity despite interspecific gene flow.

Materials and Methods

We analyzed outcomes for 1020 pregnancies observed over 46 years in a natural yellow baboon-anubis baboon hybrid zone. Fetal losses and live births were scored based on records of female reproductive state and the appearance of live neonates. We modeled the probability of fetal loss as a function of a female's genetic ancestry (the proportion of her genome estimated to be descended from anubis [vs. yellow] ancestors), age, number of previous fetal losses, dominance rank, group size, climate, and habitat quality using binomial mixed effects models.

Results

Female genetic ancestry did not predict fetal loss. Instead, the risk of fetal loss is elevated for very young and very old females. Fetal loss is most robustly predicted by ecological factors, including poor habitat quality prior to a home range shift and extreme heat during pregnancy.

Discussion

Our results suggest that gene flow between yellow and anubis baboons is not impeded by an increased risk of fetal loss for hybrid females. Instead, ecological conditions and female age are key determinants of this component of female reproductive success.     

Empirical study of hybrid zone movement

Hybrid zones are 'natural laboratories' for studying the origin, maintenance and demise of species. Theory predicts that hybrid zones can move in space and time, with significant consequences for both evolutionary and conservation biology, though such movement is often perceived as rare. Here, a review of empirical studies of moving hybrid zones in animals and plants shows 23 examples with observational evidence for movement, and a further 16 where patterns of introgression in molecular markers could be interpreted as signatures of movement. The strengths and weaknesses of methods used for detecting hybrid zone movement are discussed, including long-term replicated sampling, historical surveys, museum/herbarium collections, patterns of relictual populations and introgression of genetic markers into an advancing taxon. Factors governing hybrid zone movement are assessed in the light of the empirical studies, including environmental selection, competition, asymmetric hybridization, dominance drive, hybrid fitness, human activity and climate change. Hybrid zone movement means that untested assumptions of stability in evolutionary studies on hybrid zone can lead to mistaken conclusions. Movement also means that conservation effort aimed at protecting against introgression could unwittingly favour an invading taxon. Moving hybrid zones are of wide interest as examples of evolution in action and possible indicators of environmental change. More long-term experimental studies are needed that incorporate reciprocal transplants, hybridization experiments and surveys of molecular markers and population densities on a range of scales.     

Population genetic structure and hybridization patterns in the Mediterranean endemics Phlomis lychnitis and P. crinita (Lamiaceae)

BACKGROUND AND AIMS: The historical influence of gene flow and genetic drift after the last glacial phase of the Quaternary Period is reflected in current levels of genetic diversity and population structure of plant species. Moreover, hybridization after secondary contact might also affect population genetic diversity and structure. An assessment was made of the genetic variation and hybrid zone structure in Iberian populations of the Mediterranean Phlomis lychnitis and P. crinita, for which phylogenetic relationships are controversial, and hybridization and introgression are common. METHODS: Allozyme variation at 13 loci was analysed in 1723 individual plants sampled from 35 natural locations of P. lychnitis, P. crinita subsp. malacitana and P. crinita subsp. crinita in southern and eastern Spain. Standard genetic diversity parameters were calculated and patterns of genetic structure in each taxon were tested to fit the equilibrium between gene flow and genetic drift. Individual multilocus genotypes were subjected to Bayesian clustering analysis to estimate hybridization and introgression rates for both geographic regions. KEY RESULTS: Contrasting patterns in the distribution of genetic variation among the three taxa were found. Phlomis lychnitis showed no significant inbreeding, low genetic differentiation among populations and no evidence of isolation by distance. Phlomis crinita subsp. malacitana and P. crinita subsp. crinita showed high levels of genetic structure consistent with a pattern of gene flow-drift equilibrium. Higher instances of hybridization and introgression were detected in locations from southern Spain compared with locations from eastern Spain, matching unimodal and bimodal hybrid zones, respectively. CONCLUSIONS: High instances of historical gene flow, range expansion and altitudinal movement during the Quaternary Period, and lineage sorting can explain the diversity of patterns observed. The results suggest that P. lychnitis is the most differentiated lineage in the group; however, the relationship between the three taxa remains unclear.     

A 2000 km genetic wake yields evidence for northern glacial refugia and hybrid zone movement in a pair of songbirds

Hybrid zones are natural experiments that expose the forces maintaining species differences. But for cases where a trait of one of the hybridizing pair appears shifted into the range of the other, the underlying mechanism can be difficult to infer. For example, hybridization between hermit warbler (Dendroica occidentalis) and Townsend's warbler (Dendroica townsendi) is restricted to narrow hybrid zones in Washington and Oregon, yet hermit mtDNA can be found in phenotypically pure Townsend's populations up to 2000 km north along the Pacific coast. This could reflect introgression of selectively favoured hermit mitochondria north across the hybrid zones, or a neutral genetic wake left behind following southern zone movement. Hermit mitochondrial haplotypes in populations of coastal Townsend's exhibit relatively high genetic diversity and significant divergence from those found in populations of hermit warblers. This contradicts the predictions of selective introgression, but is consistent with a northern population of hermits diverging in a glacial refugium before being replaced by Townsend's via aggressive hybridization. Previous field studies showing Townsend's males to be competitively superior to hermit males support this scenario, and suggest that the extreme hybrid zone movement evidenced by the hermit mitochondrial wake represents an extinction in progress.     

Baboons of the amboseli basin: Demographic stability and change

A cross-sectional demographic analysis of the entire baboon population of the Amboseli basin of southern Kenya was undertaken to complement the lon-gitudinal, intensive studies of a subpopulation. The present survey documented the extent and persistence of the influx of anubis baboons into the predominantly cynocephalus community and provided another example of the nonrandom dispersal patterns of cercopithecine males. In addition, the survey confirmed continued demographic stability of the basinwide baboon population and even growth in groups that had access to better feeding conditions, despite decline of the baboons' preferred habitat and expansion of human activities into wildlife areas. Conflicts with activities of humans, however, indicate that the present well-being of the Amboseli baboon population may be short-lived.     

Genetic structure of natural populations of Castanea sativa in Turkey: evidence of a hybrid zone

This study points out the evidence of a hybrid zone between two groups of genetically differentiated populations of chestnut (Castanea sativa Mill.) in Turkey. Genetic structure, gene flow and introgression levels, based on 16 allozyme loci, were investigated on 34 population samples spanning the entire C. sativa distribution area in this country. The occurrence of the hybrid zone, located in the Bithynian region, was inferred in a group of populations showing the following genetic characteristics: (i) enhanced genetic variability and intermediate allelic frequencies between those of the Western and Eastern groups of populations; (ii) sharp and concordant changes in allele frequencies; (iii) decreased gene flow with the Western and Eastern populations. Starting from the cline width estimated to be 324 km, strength of selection was evaluated from the gene flow distance, as indicated from the degree of genetic structuring outside the hybrid zone. Evolutionary processes shaping the observed genetic differentiation and introgression are discussed on the basis of palynological data, palaeoclimatic events and evidence of hybridization found in other plant and animal species in the same region.     

Changes in the structure of the baboon hybrid zone in the Awash National Park,Ethiopia

The zone of hybridization between anubis and hamadryas baboons in the Awash National Park, Ethiopia, evidently changed significantly in the early 1970s. When first studied, by Nagel in 1968, the distribution of adult male phenotypes suggested that the hybrid zone was a narrow, static, genetic sink. In contrast, studies during the 1970s found evidence for a broad hybrid zone intergrading with parental populations and probably expanding. A more detailed investigation of data collected in 1973, presented here, shows that between 1968 and 1973 the distribution of phenotypes changed to a more clinal pattern because of the maturation and successful integration of an extensive cohort of hybrid males. We present a provisional model that accounts for the changes in terms of climatic oscillations, with the hybrid zone tending to expand during periods of climatic instability.     

Genomewide introgressive hybridization patterns in wild Atlantic salmon influenced by inadvertent gene flow from hatchery releases

Many salmonid fish populations are threatened by genetic homogenization, primarily due to introgressive hybridization with hatchery‐reared conspecifics. By applying genomewide analysis using two molecular marker types (1986 SNPs and 17 microsatellites), we assessed the genetic impacts of inadvertent gene flow via straying from hatchery releases on wild populations of Atlantic salmon in the Gulf of Finland, Baltic Sea, over 16 years (1996–2012). Both microsatellites and SNPs revealed congruent population genetic structuring, indicating that introgression changed the genetic make‐up of wild populations by increasing genetic diversity and reducing genetic divergence. However, the degree of genetic introgression varied among studied populations, being higher in the eastern part and lower in the western part of Estonia, which most likely reflects the history of past stocking activities. Using kernel smoothing and permutation testing, we detected considerable heterogeneity in introgression patterns across the genome, with a large number of regions exhibiting nonrandom introgression widely dispersed across the genome. We also observed substantial variation in nonrandom introgression patterns within populations, as the majority of genomic regions showing elevated or reduced introgression were not consistently detected among temporal samples. This suggests that recombination, selection and stochastic processes may contribute to complex nonrandom introgression patterns. Our results suggest that (i) some genomic regions in Atlantic salmon are more vulnerable to introgressive hybridization, while others show greater resistance to unidirectional gene flow; and (ii) the hybridization of previously separated populations leads to complex and dynamic nonrandom introgression patterns that most likely have functional consequences for indigenous populations.     

Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance

The primary locus of contact between free-living yellow baboons (Papio cynocephalus) in the Amboseli National Park of Kenya and the infective stages of their intestinal parasites is believed to be soil beneath sleeping trees contaminated by the baboons' own fecal emissions. In this report, we present evidence both that infective ova and larvae of intestinal parasites are found at very high densities in the soil beneath sleeping groves and that Amboseli baboons substantially reduce their contact with this reservoir of parasites by alternating periods of a few consecutive nights' use of any particular grove with much longer periods of avoidance of that grove. Although many factors other than the presence of parasite larvae also influence choice of sleeping groves, we propose as a working hypothesis that the temporal pattern of sleeping grove alternation shown by Amboseli baboons reflects a subtle behavioral strategy for parasite avoidance.     

Sociological study of a wild group of hybrid baboons betweenPapio anubis andP. hamadryas in the Awash Valley,Ethiopia

A group of hybrid baboons between anubis and hamadryas named the Gorge group was studied for five months in the Awash Valley, Ethiopia. Both morphologically and genetically, anubis features were prevalent in the Gorge group. Three types of subgroups within the group were distinguished: one-male groups, pair groups, and multi-male groups. The joining and parting of subgroups is examined by cluster-analysis. The Gorge group is concluded to be a single social unit, though it was composed of two main clusters. Grooming relations, spacing mechanisms, and sexual relations among its members were analyzed in detail. The dominance relationships among males are clarified in order to be related with their social interactions. Various aspects of the social organization are compared with those of anubis or hamadryas. It is demonstrated that the social structure of the Gorge group showed an intricate mixture of anubis and hamadryas characteristics. It is discussed how such a structure had been formed through hybridization, and what were the factors causing the differences among three types of subgroups.     

Patterns of introgression across an expanding hybrid zone: analysing historical patterns of gene flow using nonequilibrium approaches

Previous studies suggest that the hybrid zone between two taxa in the Piriqueta caroliniana complex in central Florida (south-eastern North America) has recently expanded with hybrids replacing parental genotypes across a broad region of the Florida peninsula. Here I use patterns of genetic disequilibria and levels of differentiation among populations to infer historical patterns of introgression across this broad hybrid zone. There were strong positive associations among taxon-specific alleles at the southern extent of hybridization, but disequilibria values were close to zero across the central and northern portions of the hybrid zone. Levels of among-population differentiation in the central portion of the hybrid zone were relatively low, and increased towards the northern extent of hybridization. The high levels of disequilibria are coincident with the sharp clines at the southern end of the hybrid zone, suggesting that there is a tension zone in this region that is maintained by selection against hybrids and dispersal from parental regions. The levels of disequilibria within populations and patterns of differentiation among populations are consistent with historical introgression and northward expansion of this hybrid zone, which may have slowed or ceased in recent generations.     

Mitochondrial evidence for the origin of hamadryas baboons

Baboons (Mammalia: Primates, Papio) are found primarily on the continent of Africa, but the range of hamadryas baboons (Papio hamadryas) extends to the Arabian Peninsula, and the origin of Arabian populations is unclear. To estimate the timing of the divergence between Arabian and African hamadryas populations we analyzed mitochondrial DNA (mtDNA) sequences from individuals of Arabian and African origin, and from representatives of the other major baboon taxa. The oldest hamadryas mitochondrial lineages in the Arabian Peninsula form an ancient trichotomy with the two major African lineages. This suggests that Arabia was colonized by hamadryas very soon after the appearance of the distinctive hamadryas phenotype, both events perhaps coinciding with a mid-Pleistocene stage of dry climate and low sea-level. The most closely related Arabian and African mtDNA haplotypes coalesce at approximately 35 ka, suggesting that no gene flow between African and Arabian baboons has occurred since the end of the last ice age, when a land bridge at the southern sill of the Red Sea was submerged. The mitochondrial paraphyly of Ethiopian hamadryas and anubis (P. anubis) baboons suggests an extensive and complex history of sex-specific introgression.     

Evolution of a hybrid zone of two willow species (Salix L.) in the European Alps analyzed by RAD-seq and morphometrics

Natural hybridization of plants can result in many outcomes with several evolutionary consequences, such as hybrid speciation and introgression. Natural hybrid zones can arise in mountain systems as a result of fluctuating climate during the exchange of glacial and interglacial periods, where species retract and expand their territories, resulting in secondary contacts. Willows are a large genus of woody plants with an immense capability of interspecific crossing. In this study, the sympatric area of two diploid sister species, S. foetida and S. waldsteiniana in the eastern European Alps, was investigated to study the genomic structure of populations within and outside their contact zone and to analyze congruence of morphological phenotypes with genetic data. Eleven populations of the two species were sampled across the Alps and examined using phylogenetic network and population genetic structure analyses of RAD Seq data and morphometric analyses of leaves. The results showed that a homoploid hybrid zone between the two species was established within their sympatric area. Patterns of genetic admixture in homoploid hybrids indicated introgression with asymmetric backcrossing to not only one of the parental species but also one hybrid population forming a separate lineage. The lack of F1 hybrids indicated a long-term persistence of the hybrid populations. Insignificant isolation by distance suggests that gene flow can act over large geographical scales. Morphometric characteristics of hybrids supported the molecular data and clearly separated populations of the parental species, but showed intermediacy in the hybrid zone populations with a bias toward S. waldsteiniana. The homoploid hybrid zone might have been established via secondary contact hybridization, and its establishment was fostered by the low genetic divergence of parental species and a lack of strong intrinsic crossing barriers. Incomplete ecological separation and the ability of long-distance dispersal of willows could have contributed to the spatial expansion of the hybrid zone.     

Hybridization between subspecies of waterbuck (Kobus ellipsiprymnus) in zones of overlap with limited introgression

Two subspecies of waterbuck (Kobus ellipsiprymnus), common (Kobus ellipsiprymnus ellipsiprymnus) and defassa (Kobus ellipsiprymnus defassa), are recognized based on differences in rump pattern, coat colour and geographical distribution. These forms are parapatrically distributed with an area of range overlap in East Africa, where phenotypically intermediate populations occur. Variation in 478 bp of the mitochondrial DNA control region and 14 polymorphic microsatellite loci were used to describe the genetic structure and phylogeographical pattern of the species, and to assess if the intermediate populations are the results of hybridization. In total, 186 individuals from 11 localities were analysed. A high degree of genetic differentiation was found between subspecies, although this was most evident from the microsatellite data. Hybridization was suggested in the phenotypically and geographically intermediate Nairobi NP population in Kenya. A neighbour-joining (NJ) tree based on microsatellite population genetic distances grouped Nairobi between the common and defassa populations, and a Bayesian analysis clearly showed introgression. Individuals sampled in Samburu NP, Kenya, had a common waterbuck phenotype, but introgression was suggested by both markers. Although a high degree of maternal defassa input was indicated from the sequence data, the Samburu population grouped with the common waterbuck in the microsatellite population genetic distance tree, with high support. Analyses of linkage disequilibrium and maximum-likelihood estimates of genetic drift suggested that admixture between subspecies is a recent event. The fact that introgression is limited between subspecies could be caused by chromosomal differences, hindering gene flow between common and defassa waterbuck.     

Mammalian hybrid zones: a review

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