Jacqueline M. Bishop

Molecular insight into patterns of colony composition and paternity in the common mole-rat Cryptomys hottentotus hottentotus

We report the discovery of intraspecific variation in both colony composition and patterns of paternity in two populations of the social common mole‐rat Cryptomys hottentotus hottentotus. These two populations represent the mesic and arid habitat extremes of the species’ broad ecological range in South Africa. Until recently colonies of the common mole‐rat were thought to consist of familial groups whereby all colony members were the offspring of a monogamous reproductive pair. The remaining colony members were thought to forego reproduction until both social and ecological conditions favoured dispersal and opportunities for independent outbreeding. Results from genetic assignment tests using microsatellite markers indicate that while colony composition is dominated by familial groups, colonies within both populations included both adult and subadult foreign conspecifics. Analysis of parentage reveals that the social organization of C. h. hottentotus is not that of strict monogamy; paternity of offspring was not assigned consistently to the largest, most dominant male within the colony. Moreover, a number of significantly smaller males were found to sire offspring, suggesting a sneak‐mating strategy by subordinate within‐colony males. Extra‐colony extra‐pair paternity (ECP) was also found to characterize C. h. hottentotus colonies, occurring with similar frequencies in both habitats. Both dominant established breeding males and subordinate males were identified as siring young in nonsource colonies. Furthermore, established breeding males were found to sire extra‐colony young in the same season as siring young within their source colonies. We discuss the significance of these results within the context of the divergent ecological regimes characterizing the two sites and observe that our results revisit the accuracy of using behavioural and morphological characters, which have structured the basis of our understanding of the behavioural ecology of this species, as indicators of breeding status in mark–recapture studies.

MORPHOLOGICAL AND MOLECULAR EVIDENCE REVEALS RECENT HYBRIDIZATION BETWEEN GORILLA TAXA

Molecular studies have demonstrated a deep lineage split between the two gorilla species, as well as divisions within these taxa; estimates place this divergence in the mid‐Pleistocene, with gene flow continuing until approximately 80,000 years ago. Here, we present analyses of skeletal data indicating the presence of substantial recent gene flow among gorillas at all taxonomic levels: between populations, subspecies, and species. Complementary analyses of DNA sequence variation suggest that low‐level migration occurred primarily in a westerly‐to‐easterly direction. In western gorillas, the locations of hybrid phenotypes map closely to expectations based on population refugia and riverine barrier hypotheses, supporting the presence of significant vicariance‐driven structuring and occasional admixture within this taxon. In eastern lowland gorillas, the high frequency of hybrid phenotypes is surprising, suggesting that this region represents a zone of introgression between eastern gorillas and migrants from the west, and underscoring the conservation priority of this critically endangered group. These results highlight the complex nature of evolutionary divergence in this genus, indicate that historical gene flow has played a major role in structuring gorilla diversity, and demonstrate that our understanding of the evolutionary processes responsible for shaping biodiversity can benefit immensely from consideration of morphological and molecular data in conjunction.

Why One Century of Phenetics is Enough: Response to “Are There Really Twice As Many Bovid Species As We Thought?”

1AEON—Africa Earth Observatory Network, Geoecodynamics Research Hub, c/o Department of Botany and Zoology, University of Stellenbosch, Stellenbosch 7602, South Africa; 2SARChI Chair on Biodiversity Value & Change in the Vhembe Biosphere Reserve & Core Member of Centre for Invasion Biology, School of Mathematical and Natural Sciences, University of Venda, Private Bag X5050, Thohoyandou 0950, South Africa; 3Viale Liegi 48, 00198 Roma, Italy; 4 Department of Biological Sciences, University of Cape Town, Private Bag, Rondebosch 7700, South Africa; and 5School of Archaeology and Anthropology, Australian National University, Canberra 0200, Australia; ∗Correspondence to be sent to: E-mail: fcotterill@gmail.com

Mitochondrial DNA analysis reveals Plio-Pleistocene diversification within the chacma baboon

Modern baboons evolved as a distinct lineage prior to 2.5 Mya. Previous scenarios of diversification within this lineage have assessed the phylogenetic position of the chacma baboon of southern Africa relative to other baboons, but have not examined variation within this taxon. Here we provide a phylogenetic analysis of lineage diversity across the range of the chacma baboon, and show that: (1) chacma baboons diverged as a separate lineage at approximately 1.84 Mya; (2) the chacma lineage is characterised by a deep lineage split dividing chacmas into northeastern (1.52 Mya) and southwestern (1.22 Mya) clades; (3) ruacana baboons of Namibia form their own distinct monophyletic group within the southwestern clade, emerging approximately 0.68 Mya. These patterns likely result from a complex interplay of genetic drift and gene flow as the chacma lineage diversified across a broad geographic landscape during the climatically variable Plio-Pleistocene.

Social common mole-rats enhance outbreeding via extra-pair mating

Females in many species engage in matings with males that are not their social mates. These matings are predicted to increase offspring heterozygosity and fitness, and thereby prevent the deleterious effects of inbreeding. We tested this hypothesis in a cooperative breeding mammal, the common mole-rat Cryptomys hottentotus hottentotus. Laboratory-based studies suggested a system of strict social monogamy, while recent molecular studies indicate extensive extra-pair paternity despite colonies being founded by an outbred pair. Our data show that extra-pair and within-colony breeding males differed significantly in relatedness to breeding females, suggesting that females may gain genetic benefits from breeding with non-resident males. Extra-colony male mating success was not based on heterozygosity criteria at microsatellite loci; however, litters sired by extra-colony males exhibited increased heterozygosity. While we do not have the data that refute a relationship between individual levels of inbreeding (Hs) and fitness, we propose that a combination of both male and female factors most likely explain the adaptive significance of extra-pair mating whereby common mole-rats maximize offspring fitness by detecting genetic compatibility with extra-pair mates at other key loci, but it is not known which sex controls these matings.

Phenotypic convergence in genetically distinct lineages of a Rhinolophus species complex (Mammalia, Chiroptera).

Phenotypes of distantly related species may converge through adaptation to similar habitats and/or because they share biological constraints that limit the phenotypic variants produced. A common theme in bats is the sympatric occurrence of cryptic species that are convergent in morphology but divergent in echolocation frequency, suggesting that echolocation may facilitate niche partitioning, reducing competition. If so, allopatric populations freed from competition, could converge in both morphology and echolocation provided they occupy similar niches or share biological constraints. We investigated the evolutionary history of a widely distributed African horseshoe bat, Rhinolophus darlingi, in the context of phenotypic convergence. We used phylogenetic inference to identify and date lineage divergence together with phenotypic comparisons and ecological niche modelling to identify morphological and geographical correlates of those lineages. Our results indicate that R. darlingi is paraphyletic, the eastern and western parts of its distribution forming two distinct non-sister lineages that diverged ~9.7 Mya. We retain R. darlingi for the eastern lineage and argue that the western lineage, currently the sub-species R. d. damarensis, should be elevated to full species status. R. damarensis comprises two lineages that diverged ~5 Mya. Our findings concur with patterns of divergence of other co-distributed taxa which are associated with increased regional aridification between 7-5 Mya suggesting possible vicariant evolution. The morphology and echolocation calls of R. darlingi and R. damarensis are convergent despite occupying different biomes. This suggests that adaptation to similar habitats is not responsible for the convergence. Furthermore, R. darlingi forms part of a clade comprising species that are bigger and echolocate at lower frequencies than R. darlingi, suggesting that biological constraints are unlikely to have influenced the convergence. Instead, the striking similarity in morphology and sensory biology are probably the result of neutral evolutionary processes, resulting in the independent evolution of similar phenotypes.

Sensory trait variation in an echolocating bat suggests roles for both selection and plasticity

BackgroundAcross heterogeneous environments selection and gene flow interact to influence the rate and extent of adaptive trait evolution. This complex relationship is further influenced by the rarely considered role of phenotypic plasticity in the evolution of adaptive population variation. Plasticity can be adaptive if it promotes colonization and survival in novel environments and in doing so may increase the potential for future population differentiation via selection. Gene flow between selectively divergent environments may favour the evolution of phenotypic plasticity or conversely, plasticity itself may promote gene flow, leading to a pattern of trait differentiation in the presence of gene flow. Variation in sensory traits is particularly informative in testing the role of environment in trait and population differentiation. Here we test the hypothesis of ‘adaptive differentiation with minimal gene flow’ in resting echolocation frequencies (RF) of Cape horseshoe bats (Rhinolophus capensis) across a gradient of increasingly cluttered habitats.ResultsOur analysis reveals a geographically structured pattern of increasing RF from open to highly cluttered habitats in R. capensis; however genetic drift appears to be a minor player in the processes influencing this pattern. Although Bayesian analysis of population structure uncovered a number of spatially defined mitochondrial groups and coalescent methods revealed regional-scale gene flow, phylogenetic analysis of mitochondrial sequences did not correlate with RF differentiation. Instead, habitat discontinuities between biomes, and not genetic and geographic distances, best explained echolocation variation in this species. We argue that both selection for increased detection distance in relatively less cluttered habitats and adaptive phenotypic plasticity may have influenced the evolution of matched echolocation frequencies and habitats across different populations.ConclusionsOur study reveals significant sensory trait differentiation in the presence of historical gene flow and suggests roles for both selection and plasticity in the evolution of echolocation variation in R. capensis. These results highlight the importance of population level analyses to i) illuminate the subtle interplay between selection, plasticity and gene flow in the evolution of adaptive traits and ii) demonstrate that evolutionary processes may act simultaneously and that their relative influence may vary across different environments.

Genetic signatures for enhanced olfaction in the African mole-rats.

The Olfactory Receptor (OR) superfamily, the largest in the vertebrate genome, is responsible for vertebrate olfaction and is traditionally subdivided into 17 OR families. Recent studies characterising whole-OR subgenomes revealed a ‘birth and death’ model of evolution for a range of species, however little is known about fine-scale evolutionary dynamics within single-OR families. This study reports the first assessment of fine-scale OR evolution and variation in African mole-rats (Bathyergidae), a family of subterranean rodents endemic to sub-Saharan Africa. Because of the selective pressures of life underground, enhanced olfaction is proposed to be fundamental to the evolutionary success of the Bathyergidae, resulting in a highly diversified OR gene-repertoire. Using a PCR-sequencing approach, we analysed variation in the OR7 family across 14 extant bathyergid species, which revealed enhanced levels of functional polymorphisms concentrated across the receptors’ ligand-binding region. We propose that mole-rats are able to recognise a broad range of odorants and that this diversity is reflected throughout their OR7 gene repertoire. Using both classic tests and tree-based methods to test for signals of selection, we investigate evolutionary forces across the mole-rat OR7 gene tree. Four well-supported clades emerged in the OR phylogeny, with varying signals of selection; from neutrality to positive and purifying selection. Bathyergid life-history traits and environmental niche-specialisation are explored as possible drivers of adaptive OR evolution, emerging as non-exclusive contributors to the positive selection observed at OR7 genes. Our results reveal unexpected complexity of evolutionary mechanisms acting within a single OR family, providing insightful perspectives into OR evolutionary dynamics.

Pleistocene Aridification Cycles Shaped the Contemporary Genetic Architecture of Southern African Baboons

Plio-Pleistocene environmental change influenced the evolutionary history of many animal lineages in Africa, highlighting key roles for both climate and tectonics in the evolution of Africa’s faunal diversity. Here, we explore diversification in the southern African chacma baboon Papio ursinus sensu lato and reveal a dominant role for increasingly arid landscapes during past glacial cycles in shaping contemporary genetic structure. Recent work on baboons (Papio spp.) supports complex lineage structuring with a dominant pulse of diversification occurring 1-2Ma, and yet the link to palaeoenvironmental change remains largely untested. Phylogeographic reconstruction based on mitochondrial DNA sequence data supports a scenario where chacma baboon populations were likely restricted to refugia during periods of regional cooling and drying through the Late Pleistocene. The two lineages of chacma baboon, ursinus and griseipes, are strongly geographically structured, and demographic reconstruction together with spatial analysis of genetic variation point to possible climate-driven isolating events where baboons may have retreated to more optimum conditions during cooler, drier periods. Our analysis highlights a period of continuous population growth beginning in the Middle to Late Pleistocene in both the ursinus and the PG2 griseipes lineages. All three clades identified in the study then enter a state of declining population size (Nef) through to the Holocene; this is particularly marked in the last 20,000 years, most likely coincident with the Last Glacial Maximum. The pattern recovered here conforms to expectations based on the dynamic regional climate trends in southern Africa through the Pleistocene and provides further support for complex patterns of diversification in the region’s biodiversity.

Temporal changes in allelic variation among Cape Dwarf Chameleons, Bradypodion pumilum, inhabiting a transformed, semi-urban wetland

Abstract The Cape Dwarf Chameleon, Bradypodion pumilum, is threatened by extensive habitat loss and transformation in the Western Cape Province of South Africa. As a result, the species exists as a collection of populations inhabiting an increasingly fragmented landscape within a critically endangered ecosystem. In this study we monitored microsatellite genetic variation in one of these populations of B. pumilum across a three-year period. From the results of a temporary site-vacancy of adult chameleons during the study, we anticipated a significant shift in microsatellite allele frequencies. Using data from eight highly polymorphic loci we detected differences in the allelic composition of chameleons inhabiting the study site between pre- and post-site-vacancy periods (AMOVA RST = 0.017; P = 0.019). Results suggest that recolonisation by immigrant chameleons, from an adjacent vegetation fragment connected to the study site by corridors, caused the recorded shifts in allelic frequencies. Pairwise tests of year by year comparisons revealed significant shifts in allelic frequencies between years one and two and between one and three, but not between years two and three. Our findings highlight the susceptibility of small vertebrates to stochastic changes in the allelic composition of populations in a fragmented landscape, and can be useful for the development of biodiversity management in an increasingly fragmented habitat mosaic.