Reconciling apparent conflicts between mitochondrial and nuclear phylogenies in African elephants

Conservation strategies for African elephants would be advanced by resolution of conflicting claims that they comprise one, two, three or four taxonomic groups, and by development of genetic markers that establish more incisively the provenance of confiscated ivory. We addressed these related issues by genotyping 555 elephants from across Africa with microsatellite markers, developing a method to identify those loci most effective at geographic assignment of elephants (or their ivory), and conducting novel analyses of continent-wide datasets of mitochondrial DNA. Results showed that nuclear genetic diversity was partitioned into two clusters, corresponding to African forest elephants (99.5% Cluster-1) and African savanna elephants (99.4% Cluster-2). Hybrid individuals were rare. In a comparison of basal forest "F" and savanna "S" mtDNA clade distributions to nuclear DNA partitions, forest elephant nuclear genotypes occurred only in populations in which S clade mtDNA was absent, suggesting that nuclear partitioning corresponds to the presence or absence of S clade mtDNA. We reanalyzed African elephant mtDNA sequences from 81 locales spanning the continent and discovered that S clade mtDNA was completely absent among elephants at all 30 sampled tropical forest locales. The distribution of savanna nuclear DNA and S clade mtDNA corresponded closely to range boundaries traditionally ascribed to the savanna elephant species based on habitat and morphology. Further, a reanalysis of nuclear genetic assignment results suggested that West African elephants do not comprise a distinct third species. Finally, we show that some DNA markers will be more useful than others for determining the geographic origins of illegal ivory. These findings resolve the apparent incongruence between mtDNA and nuclear genetic patterns that has confounded the taxonomy of African elephants, affirm the limitations of using mtDNA patterns to infer elephant systematics or population structure, and strongly support the existence of two elephant species in Africa.     

The conflict between humans and elephants in the central African forests

Elephants and humans each suffer from the presence of the other when they occupy the same forests. Farmers risk losing their crops to elephants, while elephants are displaced by settlements, agriculture, roads and development projects. Elephants have also been hunted for ivory. The ivory trade in the equatorial forests expanded in the nineteenth century as Europe prospered, and then again in the twentieth century as the Far East prospered. Forest elephant numbers were depleted each time.
Elephants are unpopular in the forest zone, and increasing human populations combined with the spread of democracy in central Africa pose a major threat to their future. If elephants are to be tolerated by villagers living in the equatorial forests, the costs they impose must be reduced and the benefits to the rural populace must be increased. A three-pronged strategy is suggested, involving land-use planning, measures to mitigate crop damage, and programmes to enhance the value of elephants. Elephants could be viewed as assets if their importance in the forest ecosystem were recognized, if they were domesticated for logging or transport, or if their presence was one of the factors which attracted tourists to the forest zone. However, management strategies based on hunting have the best chance of conserving elephants because of the importance of hunting in the culture of the forest people. Sport hunting for trophies may bring the greatest revenues. Community wildlife-management programmes, where village councils make the decisions, could prevent overexploitation. There are no simple answers, however, because one form of management may conflict with the goals of another.     

Contribution of molecular phylogeny and morphometrics to the systematics of African elephants

African elephants are conventionally classified as a single species: Loxodonta africana (Blumenbach 1797). However, the discovery in 1900 of a smaller form of the African elephant, spread throughout the equatorial belt of this land, has given rise to a debate over the relevance of a second species of elephant in Africa. The twentieth century has not provided any definite answer to this question. Actually, recent molecular analyses have sustained this issue by advocating either a division of forest elephants into a valid species, or their inclusion as a subspecies of L. africana. Our work initiated at the National Museum of Natural History of Paris provides new molecular (mitochondrial) and morphological (and morphometrical) evidence making it possible to propose a comprehensive phylogenetic hypothesis. It appears that there is no conclusive argument to keep forest elephants (cyclotis form) and savannah elephants (africana form) apart in two distinct species. A high level of mitochondrial introgression between the two forms, as well as a continuum in the morphology of the skulls of the two morphotypes rather suggests that, despite an ancient division, these two taxa freely interbreed wherever their ranges intersect. We thus adopt a conservative systematic position in considering these two forms as two subspecies, respectively: L. africana africana, the savannah elephant, and L. africana cyclotis, the forest elephant. We finally discuss the conservation topic in the light of this systematic framework.     

A preliminary study of the behavioral effects of feeding enrichment on African elephants

Although commonly practiced with many species, feeding enrichment in elephants is understudied. The behavioral effects of feeding enrichment were tested in three African elephants by substituting an equal dry weight of browse for hay in an ABA design. The results showed a significant increase in feeding and significant decreases in drinking and inactivity when the browse was present. Additionally, changes in feeding, inactivity, and time spent in contact were observed outside the time the browse was actually presented, although the relationship of these changes to the experimental methodology is unknown. A significant increase in visibility to zoo visitors during the browse conditions demonstrates that browse is an effective, naturalistic method for increasing visibility as well as species-typical behaviors. Managers of captive elephants should consult with a nutritionist to address issues of energetics, nutritional content, and secondary compounds when using browse as feeding enrichment. Zoo Biol 19:485-493, 2000. Copyright 2000 Wiley-Liss, Inc.     

Examination of the interrelationships of behavior,dominance status,and ovarian activity in captive Asian and African elephants

Ovarian inactivity has been identified in captive African (Loxodonta africana) and Asian (Elephas maximus) elephants and is thought to be mediated in part by social influences. Thus, a survey was conducted to determine how behavior and dominance status relate to each other and to ovarian cyclicity. For both Asian and African elephants, dominance status was positively correlated with relative size, age, temperament, disciplinary nature, and willingness to share novel objects. Relative size and temperament were also related to disciplinary nature toward herdmates. Behavior toward keepers was a good indicator of the willingness of elephants to follow commands, whereas sharing novel objects was positively correlated with object curiosity. Finally, dominance status, temperament, and disciplinary nature were all correlated with willingness to share. Comparisons of ovarian cyclicity status with behavior rankings were conducted only for African elephants because of the low number of noncycling Asian elephants surveyed. Overall, social status appeared to be the best predictor of ovarian activity in African elephants. Noncycling African elephant females ranked higher in the dominance hierarchy and gave more discipline to herdmates than cycling cohorts. It remains to be determined whether these are cause or effect relationships, but clearly it is important to understand how physical and social attributes impact physiological processes, such as reproduction. Captive management now needs to focus on optimizing social and environmental conditions to maximize reproductive potential in elephants. Zoo Biol 23:431–448, 2004. © 2004 Wiley‐Liss, Inc.     

Resource wars and conflict ivory: the impact of civil conflict on elephants in the Democratic Republic of Congo--the case of the Okapi Reserve

Human conflict generally has substantial negative impacts on wildlife and conservation. The recent civil war (1995-2006) in the Democratic Republic of Congo (DRC) resulted in a significant loss of wildlife, including elephants, due to institutional collapse, lawlessness and unbridled exploitation of natural resources such as minerals, wood, ivory and bushmeat. We used data from distance sampling surveys conducted before and after the war in a protected forest, the Okapi Faunal Reserve, to document changes in elephant abundance and distribution. We employed Generalized Additive Models to relate changes in elephant distribution to human and environmental factors. Populations declined by nearly fifty percent coinciding with a major increase in elephant poaching as indicated by reports of ivory trade during the war. Our results suggest that humans influenced elephant distribution far more than habitat, both before and after the war, but post-war models explained more of the variation. Elephant abundance declined more, closer to the park boundary and to areas of intense human activity. After the war, elephant densities were relatively higher in the centre of the park where they were better protected, suggesting that this area may have acted as a refuge. In other sites in Eastern DRC, where no protection was provided, elephants were even more decimated. Post-war dynamics, such as weakened institutions, human movements and availability of weapons, continue to affect elephants. Survival of remaining populations and recovery will be determined by these persistent factors and by new threats associated with growing human populations and exploitation of natural resources. Prioritizing wildlife protection, curbing illegal trade in ivory and bushmeat, and strengthening national institutions and organizations in charge of conservation will be crucial to counter these threats.     

Studying sources of incongruence in arthropod molecular phylogenies: Sea spiders (Pycnogonida) as a case study

In this report, we analyze the phylogeny of Pycnogonida using the three nuclear and three mitochondrial markers currently sequenced for studying inter- and intrafamilial relationships within Arthropoda: 18S and 28S rRNA genes, Histone H3, cytochrome c oxidase subunit 1 (CO1), 12S and 16S rRNA genes. We identify several problems in previous studies, due to the use of inappropriate sequences (taxonomic misidentification, DNA contamination, sequencing errors, missing data) or taxa (outgroup choice). Our analyses show that most markers are not powerful to study the phylogeny of sea spiders. The results suggest however a recent diversification of the group (Mesozoic rather than Paleozoic) and the early divergence of Austrodecidae, followed by Colossendeidae, Pycnogonidae and Rhynchothoracidae. Except Ammotheidae and Callipallenidae, all other families were recovered as monophyletic. Analyses of synonymous sites in CO1 sequences reveal an extreme heterogeneity of nucleotide composition within sea spiders, as six unrelated species show a reverse strand-specific bias. We therefore suggest that several independent reversals of asymmetric mutational constraints occurred during the evolution of Pycnogonida, as a consequence of genomic inversions involving either the control region or a fragment containing the CO1 gene. These hypotheses are supported by the comparison of two complete mitochondrial genomes of sea spiders (Achelia bituberculata and Nymphon gracile) with that of Limulus.     

Testing the relationship between morphological and molecular rates of change along phylogenies

Abstract.— Molecular evolution has been considered to be essentially a stochastic process, little influenced by the pace of phenotypic change. This assumption was challenged by a study that demonstrated an association between rates of morphological and molecular change estimated for "total-evidence" phylogenies, a finding that led some researchers to challenge molecular date estimates of major evolutionary radiations. Here we show that Omland's (1997) result is probably due to methodological bias, particularly phylogenetic nonindependence, rather than being indicative of an underlying evolutionary phenomenon. We apply three new methods specifically designed to overcome phylogenetic bias to 13 published phylogenetic datasets for vertebrate taxa, each of which includes both morphological characters and DNA sequence data. We find no evidence of an association between rates of molecular and morphological rates of change.     

A molecular phylogenetic study of southern African Apiaceae

It has been suggested that southern Africa is the origin of the predominantly herbaceous Apiaceae subfamily Apioideae and that the woody habit is plesiomorphic. We expand previous molecular phylogenetic analyses of the family by considering all but three of the approximately 38 genera native to southern Africa, including all genera whose members, save one, have a woody habit. Representatives of five other genera are included because they may be closely related to these southern African taxa. Chloroplast DNA rps16 intron and/or nuclear rDNA ITS sequences for 154 accessions are analyzed using maximum parsimony, Bayesian, and maximum likelihood methods. Within Apioideae, two major clades hitherto unrecognized in the subfamily are inferred. The monogeneric Lichtensteinia clade is sister group to all other members of the subfamily, whereas the Annesorhiza clade (Annesorhiza, Chamarea, and Itasina) plus Molopospermum (and Astydamia in the ITS trees) are the successive sister group to all Apioideae except Lichtensteinia. Tribe Heteromorpheae is expanded to include Pseudocarum, "Oreofraga" ined., and five genera endemic to Madagascar. The southern African origin of subfamily Apioideae is corroborated (with subsequent migration northward into Eurasia along two dispersal routes), and the positions of the herbaceous Lichtensteinia and Annesorhiza clades within the subfamily suggest, surprisingly, that its ancestor was herbaceous, not woody.     

Dating nodes on molecular phylogenies: a critique of molecular biogeography

Taxa have been dated using three methods: equating their age with the age of the oldest known fossil, with the age of strata the taxa are endemic to, and with the age of paleogeographic events. All three methods have been adopted as methods of dating nodes in molecular phylogenies. The first method has been the most popular, but both this and the second method involve serious difficulties. Studies often, correctly, introduce oldest known fossils as providing minimum ages for divergences. However, in the actual analyses these ages, and ages derived from them, are often treated as absolute ages and earlier geological events are deemed irrelevant to the phylogeny. In fact, only younger geological events can be irrelevant. Studies correlating the age of nodes with age of volcanic islands often overlook the fact that these islands have been produced at subduction zones or hot spots where small, individually ephemeral islands are constantly being produced and disappearing, and a metapopulation can survive indefinitely. Correlating the age of taxa with that of associated paleogeographic events is probably the most promising method but has often been used in a simplistic way, for example in assuming that all divergence across the Isthmus of Panama dates to its final rise. Most workers now agree that a global molecular clock does not exist, and that rates can change between lineages and within a lineage over time. New methods of estimating branch lengths do not assume a strict clock, but the number of models for molecular evolution is then effectively infinite. Problems with calibrating the nodes, as well as with substitution models, mean that phylogeography's claim to be able to test between vicariance and dispersal is not justified. © The Willi Hennig Society 2005.     

On the genetic interrelationships of South African Negroes

This study addresses the comparative genetic interrelationships between South African Negro groups. For this the genetic distances between seven ethnically defined Negro subsamples (total of 998 individuals) based on 24 genetic loci/polymorphisms are calculated by applying standard distance formulae. These computations offer an opportunity to evaluate the different polymorphisms in terms of their effects on the genetic distances. The genetic interrelationships thus computed are illustrated by way of dendrograms and are discussed in terms of their comparative significance. It follows from the findings that the Ndebele, Northern Sotho (Pedi), and Tswana form a closely related subcluster and that the Zulu and Swazi as well as the Venda and Shangana-Tsonga form two additional, more distant, subclusters. These results are discussed and tentatively interpreted against the background of the reported Khoisan admixture of the populations concerned as well as their ethnological history. The data are also compared to those derived from metric and dermatoglyphic studies. It is concluded that whereas there is some agreement between these categories of variation (genetic, metric, and dermatoglyphic) as far as the comparative evaluation of South African Negro groups is concerned, there also are discrepancies. These conclusions need to be explained in terms of evolutionary mechanisms (such as historic origins, hybridization, natural selection, and genetic drift) in order to obtain a more consistent and comprehensive comparative picture of the physical anthropology of southern African populations.     

Ichthyofaunal assemblages in estuaries: A South African case study

This review places the life-history styles of fishes associated with South African estuaries in a global context and presents a classification system incorporating all the major life-history categories for estuary-associated fish species around the world. In addition, it documents the early life histories of the major fish groups in South African estuaries, with particular emphasis on the differing modes of estuarine utilization by marine, estuarine and freshwater taxa.This review details factors influencing the ichthyofaunal community structure in South African estuaries. The availability of fish for recruitment into an estuary depends primarily upon the distributional range of euryhaline marine and estuarine species, with tropical and temperate taxa showing marked abundance trends. Within a particular biogeographic region, however, estuarine type and prevailing salinity regime have a major influence on the detailed ichthyofaunal structure that develops. There is an increasing preponderance of marine fish taxa when moving from a freshwater-dominated towards a seawater-dominated type of system, and a decline in species diversity between subtropical estuaries in the north-east and cool temperate systems in the south-west. Similar declines in fish species diversity between tropical and temperate estuaries in other parts of the world are highlighted.Fish assemblages in estuaries adjust constantly in response to changing seasons, salinities, turbidities, etc. Despite persistent fluctuations in both the biotic and abiotic environment, the basic ichthyofaunal structure appears to have an underlying stability and to be predictable in terms of the response of individual species to specific conditions. This stability seems to be governed by factors such as the dominance of eurytopic taxa within estuarine assemblages and the robust nature of food webs within these systems. The predictability arises from factors such as the seasonality associated with estuarine spawning cycles and juvenile fish recruitment patterns. These patterns, together with a well-documented resilience to a wide range of physico-chemical and biotic perturbations, appear to be an underlying feature of fish assemblages in estuaries around the world.In contrast to marine fish species, estuary-associated taxa have received little conservation attention. Apart from the designation of protected areas, the main direct means of conserving estuary-associated fish stocks include habitat conservation and controls over fishing methods, effort, efficiency and seasonality. Of these, the conservation of fish habitats, the most important, because healthy aquatic environments invariably support healthy fish populations. The use of estuarine sanctuaries for fish conservation is briefly reviewed, as well as the legislation governing the USA National Estuarine Research Reserve System (NERRS) and the Australian Marine and Estuarine Protected Area (MEPA) system. It is concluded that South Africa requires an expansion of the existing Estuarine Protected Area (EPA) network, as well as the upgrading of selected 'estuarine reserves' where fishing is permitted, into 'estuarine sanctuaries' where no exploitation of biological resources is allowed.     

Gymnogrammitis dareiformis is a polygrammoid fern (Polypodiaceae) – Resolving an apparent conflict between morphological and molecular data

 Maximum parsimony and maximum likelihood analyses of the combined data sets of two chloroplast genes, rbcL and rps4, demonstrate that nk;the monotypic genus Gymnogrammitis is part of the polygrammoid clade (Polypodiaceae + Grammitidaceae), and not the Davalliaceae as proposed in most studies. The genus forms a clade together with two Asiatic genera of the Polypodiaceae, Arthromeris and Selliguea. These last two genera have either simple or once-pinnate leaves, whereas Gymnogrammitis has highly divided (3- to 4-pinnate) blades. Two characters of this genus, the basic chromosome number of x=36 and the absence of indusia, support a relationship with the Polypodiaceae. Neither feature is found within Davalliaceae. Three morphological characters support the placement of Gymnogrammitis within the selligueoid lineage of Polypodiaceae: spores with a thick perine extending in microspines, sclerenchymatous strands in the rhizome, and non-clathrate rhizome scales. These results demonstrate that molecular and morphological data are phylogenetically congruent with the exception of blade dissection. Our study clearly shows the pitfalls of classifications based on single characters, and illustrates the importance of phylogenetic assessment of all taxonomic conclusions. Received November 22, 2001; accepted May 21, 2002 Published online: November 14, 2002 Addresses of the authors: Harald Schneider (e-mail: hschneid@duke.edu), Department of Biology, Duke University, Durham, North Carolina, 27708, USA; Current address: Albrecht-von-Haller Institut für Pflanzenwissenschaften der Universit?t G?ttingen, Abteilung Systematische Botanik, Untere Karspüle 2, D-37073 G?ttingen, Germany. Alan R. Smith, Ray Cranfill, University Herbarium, University of California, Berkeley, California 94720-2465, USA. Christopher H. Haufler, Terri Hildebrand, Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045, USA. Tom A. Ranker, University Museum and Department of Environmental, Population, and Organismic Biology, University of Colorado, Boulder, Colorado 80309, USA.     

A molecular analysis of the interrelationships of tetraodontiform fishes (Acanthomorpha: Tetraodontiformes)

Tetraodontiform fishes (e.g., triggerfishes, boxfishes, pufferfishes, and giant ocean sunfishes) have long been recognized as a monophyletic group. Morphological analyses have resulted in conflicting hypotheses of relationships among the tetraodontiform families. Molecular data from the single-copy nuclear gene RAG1 and from two mitochondrial ribosomal genes, 12S and 16S, were used to test these morphology-based hypotheses. Total evidence (RAG1+12S+16S), RAG1-only, and mitochondrial-only analyses were performed using both maximum parsimony and Bayesian criteria. Total evidence and RAG1-only analyses recover a monophyletic Tetraodontiformes. However, the relationships recovered within the order differ, and none completely conform to previous hypotheses. Analysis of mitochondrial data alone fails to recover a monophyletic Tetraodontiformes and therefore does not support any of the morphology-based topologies. The RAG1 data appear to give the best estimate of tetraodontiform phylogeny, resulting in many strongly supported nodes and showing a high degree of congruence between both parsimony and Bayesian analyses. All analyses recover every tetraodontiform family for which more than one representative is included as a strongly supported monophyletic group. Balistidae and Monacanthidae are recovered as sister groups with robust support in every analysis, and all analyses except the Bayesian analyses of the mitochondrial data alone recover a strongly supported sister-group relationship between Tetraodontidae and Diodontidae. Many of the intrafamilial relationships recovered from the molecular data presented here corroborate previous morphological hypotheses.     

Parent-offspring conflict: A case of arrested development

The theory of parent-offspring conflict (POC) provides a plausible evolutionary foundation for the dissonant behavioral interactions commonly observed between adults and their progeny. It has been modelled extensively, but its predictions for phenotypes are murky and have been subjected to scant empirical testing. The least ambiguous cases are likely to involve taxa where offspring exert real power. Recent experimental work indicates that worker bees manipulate brood sex ratios differently from the queen. By contrast, most studies of avian brood reduction and mammalian ‘weaning conflict’ remain open to multiple interpretations. In general, POC may owe its current hegemony to the paucity of alternative explanations for parent-offspring squabbles. Reassessments of basic assumptions about what both parties ‘really want’ need to be linked to experimentation, field-oriented modelling and pluralism for this provocative theory to become broadly useful.