Sequential Fragmentation of Pleistocene Forests in an East Africa Biodiversity Hotspot: Chameleons as a Model to Track Forest History

CITATION: Measey, G. J. & Tolley, K. A. 2011. Sequential fragmentation of Pleistocene forests in an East Africa biodiversity hotspot : chameleons as a model to track forest history. PLoS ONE, 6(10): e26606, doi:10.1371/journal.pone.0026606.The original publication is available at http://journals.plos.org/plosoneBackground The Eastern Arc Mountains (EAM) is an example of naturally fragmented tropical forests, which contain one of the highest known concentrations of endemic plants and vertebrates. Numerous paleo-climatic studies have not provided direct evidence for ancient presence of Pleistocene forests, particularly in the regions in which savannah presently occurs. Knowledge of the last period when forests connected EAM would provide a sound basis for hypothesis testing of vicariance and dispersal models of speciation. Dated phylogenies have revealed complex patterns throughout EAM, so we investigated divergence times of forest fauna on four montane isolates in close proximity to determine whether forest break-up was most likely to have been simultaneous or sequential, using population genetics of a forest restricted arboreal chameleon, Kinyongia boehmei. Methodology/Principal Findings We used mitochondrial and nuclear genetic sequence data and mutation rates from a fossil-calibrated phylogeny to estimate divergence times between montane isolates using a coalescent approach. We found that chameleons on all mountains are most likely to have diverged sequentially within the Pleistocene from 0.93–0.59 Ma (95% HPD 0.22–1.84 Ma). In addition, post-hoc tests on chameleons on the largest montane isolate suggest a population expansion ∼182 Ka. Conclusions/Significance Sequential divergence is most likely to have occurred after the last of three wet periods within the arid Plio-Pleistocene era, but was not correlated with inter-montane distance. We speculate that forest connection persisted due to riparian corridors regardless of proximity, highlighting their importance in the region's historic dispersal events. The population expansion coincides with nearby volcanic activity, which may also explain the relative paucity of the Taita's endemic fauna. Our study shows that forest chameleons are an apposite group to track forest fragmentation, with the inference that forest extended between some EAM during the Pleistocene 1.1–0.9 Ma.http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0026606Publisher's versio

Sexual dimorphism in bite performance drives morphological variation in chameleons

Phenotypic performance in different environments is central to understanding the evolutionary and ecological processes that drive adaptive divergence and, ultimately, speciation. Because habitat structure can affect an animal's foraging behaviour, anti-predator defences, and communication behaviour, it can influence both natural and sexual selection pressures. These selective pressures, in turn, act upon morphological traits to maximize an animal's performance. For performance traits involved in both social and ecological activities, such as bite force, natural and sexual selection often interact in complex ways, providing an opportunity to understand the adaptive significance of morphological variation with respect to habitat. Dwarf chameleons within the Bradypodion melanocephalum-Bradypodion thamnobates species complex have multiple phenotypic forms, each with a specific head morphology that could reflect its use of either open-or closed-canopy habitats. To determine whether these morphological differences represent adaptations to their habitats, we tested for differences in both absolute and relative bite performance. Only absolute differences were found between forms, with the closed-canopy forms biting harder than their open-canopy counterparts. In contrast, sexual dimorphism was found for both absolute and relative bite force, but the relative differences were limited to the closed-canopy forms. These results indicate that both natural and sexual selection are acting within both habitat types, but to varying degrees. Sexual selection seems to be the predominant force within the closed-canopy habitats, which are more protected from aerial predators, enabling chameleons to invest more in ornamentation for communication. In contrast, natural selection is likely to be the predominant force in the open-canopy habitats, inhibiting the development of conspicuous secondary sexual characteristics and, ultimately, enforcing their overall diminutive body size and constraining performance

Mind the gaps: investigating the cause of the current range disjunction in the Cape Platanna, Xenopus gilli (Anura: Pipidae)

Low-lying areas of the Cape at Africa’s south-westernmost tip have undergone dramatic marine-remodelling, with regular changes in sea-level following glacial cycles. Species for which marine barriers are impenetrable underwent concomitant radical distribution changes which may account for current range disjunctions. The Cape platanna, Xenopus gilli, is a frog distributed in only three disjunt areas within low-lying regions of the southwestern Cape. We determined the relationship between frogs from these three disjunct areas, by using a combination of morphometric analysis and mtDNA (ND2 and 16S fragments) sequences of 130 frogs from eight ponds. Coalescent analyses on molecular data dated the divergence in two major clades to around 4.6 Mya, a period during which major uplifting on the eastern side of the subcontinent caused climate changes throughout southern Africa. Principal components analysis showed significant morphometric differences between each clade on head and limb measurements. Consistent differences in ventral colouration and patterning were also observed. We report on increased levels of hybridisation with X. laevis throughout the range of X. gilli, which reaches at least 27% hybrids in some ponds. Urgent conservation actions are required to control habitat loss from alien invasive vegetation, and prevent introgression with the domestic-exotic, X. laevis

Frog origins: inferences based on ancestral reconstructions of locomotor performance and anatomy

Frogs are the most species-rich and ecologically diverse group of amphibians and are characterized by a unique body plan including long legs, elongated ilia, and fused caudal vertebrae. Stem anurans such as Triadobatrachus or Czatkobatrachus have been suggested to have used jumping or hopping as part of their locomotor repertoire based on their anatomy. The earliest known true frog, Prosalirus bitis was suggested to have been a proficient jumper. However, data on jumping performance in frogs have never been used to attempt reconstruction of ancestral features at the base of the radiation. Here we provide data on jumping performance (forces and acceleration) in 20 species of extant frogs including representatives of most of the early radiating clades. We next use ancestral character value inferences to assess ancestral features. Our analyses suggest that frog ancestors were of small to medium size, had relatively short limbs, produced rather low jump forces, yet were capable of relatively high acceleration. Given the short limbs and low forces, the unique frog bauplan with a reduced vertebral column and a mobile ilio-sacral joint may not have been an adaptation for powerful jumping

Patterns of geographic variation between mitochondrial and nuclear markers in Heaviside’s (Benguela) dolphins (Cephalorhynchus heavisidii)

The Heaviside's (or Benguela) dolphin (Cephalorhynchus heavisidii) is endemic to the west coast of southern Africa. The present study investigated the population genetic structure across a large portion of the species distribution using mitochondrial control region and nuclear (microsatellite) markers. A total of 395 biopsy skin samples were analyzed; they were collected from free‐ranging Heaviside's dolphins in 7 locations along 1650 km of coast between Table Bay, South Africa and Walvis Bay, Namibia. Both genetic markers rejected the hypothesis of 1 homogenous population but revealed contrasting results in the genetic structuring of putative populations. Mitochondrial DNA suggested either 2 populations or a fine‐scale division with 6 (sub) populations, while microsatellite markers were indicative of 2 widespread populations with measurable gene flow between them. Neutrality tests and mismatch distribution of the mitochondrial sequences indicated a departure from mutation–drift equilibrium due to a population expansion at the 2 extremes of the geographic range, but not towards the middle of the distribution. These results highlight the importance of evaluating multiple genetic markers to gain reliable insights into population processes and structure.Supplementary material: Table S1 Summary of genetic variation based on 16 microsatellite loci in the Heaviside's dolphin: Ta stands for annealing temperature, bp for allele sizes, and Na represents the number of alleles examined within each putative population where observed (HO) and expected (HE) heterozygosities were estimated; n indicates the number of individuals used in calculations; dash (−) indicates loci which were not polymorphic, PI stands for Probability of Identity per locus, and PIsibs indicates Probability of Identity for genetic similarity among siblings per locus. Locus SCA22 did not amplify and loci Dde09 and Dde059 were monomorphic Table S2 Genetic variability estimates in mtDNA control region sequences excluding singletons (n = 27) for haplotype diversity (h) and nucleotide diversity (π) Table S3 Summary of genetic variation based on 13 microsatellite loci in the Heaviside's dolphin: Na indicates the number of alleles examined per each sampling site where observed (HO) and expected (HE) heterozygosities were estimated, HWE stands for Hardy‐Weinberg equilibrium; n indicates the number of individuals used in calculations, § denotes loci out of HWE (≤0.05) and ∗ indicates evidence for null allele. Locus SCA22 did not amplify and loci Dde09 and Dde059 were monomorphic Table S4 Sex‐biased dispersal results for males and females with respect to FIS, FST, HO, HS, mean assignment and variance assignment Table S5 Haplotype frequencies per sampling location of 51 haplotypes identified in biopsy samples of Heaviside's dolphins obtained at seven locations off the southwest African coast Table S6 STRUCTURE clustering analysis: a. Proportion of Heaviside's dolphin individuals from each of the seven sampling locations assigned to each of the two clusters inferred from STRUCTURE analysis Figure S1 Median‐joining network of mtDNA control region haplotypes without singletons for Heaviside's dolphins found off the southwest coast of southern Africa. Figure S2 Average posterior probability (ln K) for each of the seven clusters (i.e., K 1 to 7) from 15 independent runs. Figure S3 Log‐likelihood values (Ln Pr(X/K)) from 15 independent runs, where the ad hoc statistic delta K (ΔK) shows the most probable number of genetic clusters (K). Figure S4 Bayesian assignment probabilities where K = 6 clusters were inferred from STRUCTURE analysis. Two sampling sites, Hondeklipbaai and Port Nolloth, are grouped together as in the AMOVA results using mtDNA control region data. Each individual is represented by a thin vertical line, which is portioned into K coloured segments that represent the individual's estimated membership fractions in K clusters. Black lines separate individuals of different populations. The six putative populations are labelled below the figure.The National Research Foundation (NRF) of South Africa, the Kate Sanderson Bequest Fund administered by the Internation-al Union for Conservation of Nature (IUCN), the South African National Biodiversity Institute-Threatened Spe-cies Programme, the Andrew W. Mellon Foundation and the Rufford Small Grants Foundation.https://onlinelibrary.wiley.com/journal/174948772020-09-01hj2020Mammal Research Institut

Refinement of locality data for FitzSimons’ Garter Snake Elapsoidea sundevallii fitzsimonsi Loveridge, 1948 provides a better estimation of its distribution

Foundational data on species taxonomy, distribution and ecology forms the basis of assessing species for their conservation status. For African reptiles, distributional data are sorely lacking for many taxa, sometimes resulting in inadequate conservation assessments (Tolley et al., 2016). In South Africa, some geographic areas are poorly sampled with gaps exceeding 15,000 km2 in which there are no locality records (see Branch, 2014) and the implications of this could be considerable in terms of assessing species for extinction risk. To address these information gaps, we surveyed in the poorly sampled arid western Kalahari region of North West Province, South Africa during 2019

Phylogeny and phylogeography of chelonians from sub-Saharan Africa—A review of current knowledge in tribute to Margaretha D. Hofmeyr

Species-level phylogeny and especially phylogeography of African chelonians is a comparatively under-studied field of research. We review the current knowledge of phylogeny and phylogeography, highlight congruence of spatial phylogeographic patterns amongst chelonians and other taxa and suggest future research directions to address gaps in knowledge. Our review shows that phylogeographic and phylogenetic investigations have led to unexpected findings. For example, for Pelomedusa, a putatively wide-ranging monotypic terrapin genus, cryptic diversity was revealed, with more than ten species being uncovered. The formerly recognized tortoise genus Homopus sensu lato was found to be paraphyletic with respect to Chersina. To resolve this situation, Homopus was restricted to the four-toed species H. areolatus and H. femoralis and the genus Chersobius was resurrected for the five-toed species C. boulengeri, C. signatus, and C. solus. Three previously recognized taxa were shown to be invalid, viz. the putatively extinct terrapin species Pelusios seychellensis and the tortoise subspecies Chersobius signatus cafer and Stigmochelys pardalis babcocki. Together with taxonomy, the knowledge of phylogeographic structuring sets a solid foundation for conservation measures and allows the identification of Management and Conservation Units. However, the current legislation, in particular the enforcement of the Nagoya Protocol under the Convention of Biological Diversity (CBD), has largely halted research on widely distributed taxa and turned the well-intended concept of Access and Benefit Sharing into a major impediment for conservation and research. The current situation leads for many species to a continued usage of outdated and incorrect taxonomic classifications resulting in an error cascade of conservation decisions. This is counterproductive to the aims of the CBD, that is, the protection of biodiversity. Sequencing historical DNA from museum specimens using aDNA approaches could be a short-term approach to mitigate, but not solve, this impediment

Long-term feeding ecology and habitat use in harbour porpoises Phocoena phocoena from Scandinavian waters inferred from trace elements and stable isotopes

BACKGROUND: We investigated the feeding ecology and habitat use of 32 harbour porpoises by-caught in 4 localities along the Scandinavian coast from the North Sea to the Barents Sea using time-integrative markers: stable isotopes (δ(13)C, δ(15)N) and trace elements (Zn, Cu, Fe, Se, total Hg and Cd), in relation to habitat characteristics (bathymetry) and geographic position (latitude). RESULTS: Among the trace elements analysed, only Cd, with an oceanic specific food origin, was found to be useful as an ecological tracer. All other trace elements studied were not useful, most likely because of physiological regulation and/or few specific sources in the food web. The δ(13)C, δ(15)N signatures and Cd levels were highly correlated with each other, as well as with local bathymetry and geographic position (latitude). Variation in the isotopic ratios indicated a shift in harbour porpoise's feeding habits from pelagic prey species in deep northern waters to more coastal and/or demersal prey in the relatively shallow North Sea and Skagerrak waters. This result is consistent with stomach content analyses found in the literature. This shift was associated with a northward Cd-enrichment which provides further support to the Cd 'anomaly' previously reported in polar waters and suggests that porpoises in deep northern waters include Cd-contaminated prey in their diet, such as oceanic cephalopods. CONCLUSION: As stable isotopes and Cd provide information in the medium and the long term respectively, the spatial variation found, shows that harbour porpoises experience different ecological regimes during the year along the Scandinavian coasts, adapting their feeding habits to local oceanographic conditions, without performing extensive migration

Exploration into the hidden world of Mozambique’s sky island forests:new discoveries of reptiles and amphibians

We carried out a survey of reptiles and amphibians within Afromontane forest and woodland slopes of three inselbergs in northern Mozambique (Mount Mabu, Mount Namuli, and Mount Ribáuè). A total of 56 species (22 amphibians and 34 reptiles) were recorded during the current survey. Our findings substantially increase the number of herpetofaunal species recorded from these mountains (Mount Ribáuè 59%, Mount Mabu 37%, and Mount Namuli 11% of the total species), including one new country record and several putative new species. An updated checklist of the herpetofauna of these mountains is presented

A multilocus phylogeny of the world Sycoecinae fig wasps (Chalcidoidea: Pteromalidae)

The Sycoecinae is one of five chalcid subfamilies of fig wasps that are mostly dependent on Ficus inflorescences for reproduction. Here, we analysed two mitochondrial ( COI , Cyt b ) and four nuclear genes (ITS2, EF-1α, RpL27a, mago nashi ) from a worldwide sample of 56 sycoecine species. Various alignment and partitioning strategies were used to test the stability of major clades. All topologies estimated using maximum likelihood and Bayesian methods were similar and well resolved but did not support the existing classification. A high degree of morphological convergence was highlighted and several species appeared best described as species complexes. We therefore proposed a new classification for the subfamily. Our analyses revealed several cases of probable speciation on the same host trees (up to 8 closely related species on one single tree of F. sumatrana ), which raises the question of how resource partitioning occurs to avoid competitive exclusion. Comparisons of our results with fig phylogenies showed that, despite sycoecines being internally ovipositing wasps host-switches are common incidents in their evolutionary history. Finally, by studying the evolutionary properties of the markers we used and profiling their phylogenetic informativeness, we predicted their utility for resolving phylogenetic relationships of Chalcidoidea at various taxonomic levels