Bert Van Bocxlaer

Old fossils–young species: evolutionary history of an endemic gastropod assemblage in Lake Malawi

Studies on environmental changes provide important insights into modes of speciation, into the (adaptive) reoccupation of ecological niches and into species turnover. Against this background, we here examine the history of the gastropod genus Lanistes in the African Rift Lake Malawi, guided by four general evolutionary scenarios, and compare it with patterns reported from other endemic Malawian rift taxa. Based on an integrated approach using a mitochondrial DNA phylogeny and a trait-specific molecular clock in combination with insights from the fossil record and palaeoenvironmental data, we demonstrate that the accumulation of extant molecular diversity in the endemic group did not start before approximately 600 000 years ago from a single lineage. Fossils of the genus from the Malawi Rift, however, are over one million years older. We argue that severe drops in the lake level of Lake Malawi in the Pleistocene offer a potential explanation for this pattern. Our results also challenge previously established phylogenetic relationships within the genus by revealing parallel evolution and providing evidence that the endemic Lanistes species are not restricted to the lake proper but are present throughout the Malawi Rift.

Comparison of morphometric techniques for shapes with few homologous landmarks based on machine-learning approaches to biological discrimination

Abstract Biometric analyses are useful tools for the study of organisms, their phylogenetic affiliation, and the pattern and rate of their evolution. Various morphometric techniques have been developed to analyze morphological variation, but methodological choices are often made arbitrarily because quantitative comparisons are lacking or inconclusive. Here we address morphometric quantification of taxa with few unambiguously identifiable landmarks (<15), utilizing ornamented and unornamented gastropod shells. Support vector machines were applied to evaluate classification performances of landmark (LMA), elliptic Fourier (EFA), and semi-landmark analysis (SLM). This evaluation is based on the discrimination of between-group differences relative to within-group variation, and thus allows comparing how the techniques treat different types of biological information. The results suggest that EFA performs slightly better than SLM (and certainly LMA) in discerning a priori identified taxa with unornamented shells, but that SLM is significantly superior to other techniques for ornamented shells. Alignment and homology problems may cause the subtle variations in ornamentation to become blurred as noise in EFA, even though EFA is often cited to be able to deal with complex shapes. Performance of LMA depends entirely on how accurately the structure can be covered with landmarks. Guidelines in choosing a morphometric technique in diverse cases are provided.

GRADUAL VERSUS PUNCTUATED EQUILIBRIUM EVOLUTION IN THE TURKANA BASIN MOLLUSCS: EVOLUTIONARY EVENTS OR BIOLOGICAL INVASIONS?

Abstract A running controversy in evolutionary thought was Eldredge and Goulds punctuated equilibrium model, which proposes long periods of morphological stasis interspersed with rapid bursts of dramatic evolutionary change. One of the earliest and most iconic pieces of research in support of punctuated equilibrium is the work of Williamson on the Plio-Pleistocene molluscs of the Turkana Basin. Williamson claimed to have found firm evidence for three episodes of rapid evolutionary change separated by long periods of stasis in a high-resolution sequence. Most of the discussions following this report centered on the topics of (eco)phenotypy versus genotypy and the possible presence of preservational and temporal artifacts. The debate proved inconclusive, leaving Williamsons reports as one of the empirical foundations of the paradigm of punctuated equilibrium. Here we conclusively show Williamsons original interpretations to be highly flawed. The supposed rapid bursts of punctuated evolutionary change represent artifacts resulting from the invasion of extrabasinal faunal elements in the Turkana palaeolakes during wet phases well known from elsewhere in Africa.

Freshwater Molluscs of the Nile Basin, Past and Present

The malacofauna of the Nile is poor compared to that of the Congo and its degree of endemicity is lower. While the highest species richness of the Congo Basin is in stenotopic taxa that live in the rivers and lakes, the highest diversity in the Nile Basin occurs in eurytopic taxa living in fringe habitats such as temporary pools. The paucity of endemics that need perennial waters as well in the Lower Nile as in the White Nile confirms the geological evidence indicating instability and discontinuity in water supply during Plio-Pleistocene times. The fauna of the Nile is predominantly Afrotropical in the Lower Nile and exclusively Afrotropical south of the junction of the White Nile and Blue Nile. Of all sub-basins, the degree of endemicity (either zero or two species) is lowest in the Equatorial Nile, indicating that the perennial aquatic environment in this sub-basin is young (probably Holocene) and lending support to the idea that the Bahr el Arab and White Nile Transcontinental Rift System were hydrologically unstable, with endorheic, alkaline lakes during most of the Plio-Pleistocene (Salama, 1997). In the Lower (Egyptian) Nile and in the Ethiopian Highlands palaearctic faunal components occur, consisting of widespread species and of a limited number of endemics of palaearctic origin, related to Levantine species. Most of these taxa first appear in the fossil record around 2.5 Ma. There is no evidence that the Nile functioned as an invasion route for Eurasiatic species prior to that time. Only Theodoxus niloticus is possibly of Paratethyan origin and may have invaded in the Late Miocene. The main invasion of freshwater molluscs into Africa appears to have occurred via the Horn of Africa in Middle and Late Miocene times. In the East African Rift, a diversified fauna occurs that only shares a fraction of species with the Nile Basin north of the Albert Nile (> ∼5° N). In the equato- rial headwaters, some species from southern Africa reach their northern limit, but the main community consists of species that are either endemic to one of the rift lakes or endemic to the region stretching from Turkana to the Kivu Basins. There hence exists a distinct East African bio-province, that was already recognisable in

Morphological stasis in an ongoing gastropod radiation from Lake Malawi

Evolutionary processes leading to adaptive radiation regularly occur too fast to be accurately recorded in the fossil record but too slowly to be readily observed in living biota. The study of evolutionary radiations is thereby confronted with an epistemological gap between the timescales and approaches used by neontologists and paleontologists. Here we report on an ongoing radiation of extant Bellamya species (n = 4) from the African Rift Lake Malawi that provides an unusual opportunity to bridge this gap. The substantial molecular differentiation in this monophyletic Bellamya clade has arisen since Late Pleistocene megadroughts in the Malawi Basin caused by climate change. Morphological time-series analysis of a high-resolution, radiocarbon-dated sequence of 22 faunas spanning the Holocene documents stasis up to the middle Holocene in all traits studied (shell height, number of whorls, and two variables obtained from geometric morphometrics). Between deposition of the last fossil fauna (∼5 ka) and the present day, a drastic increase in morphological disparity was observed (3.7–5.8 times) associated with an increase in species diversity. Comparison of the rates of morphological evolution obtained from the paleontological time-series with phylogenetic rates indicates that the divergence in two traits could be reconstructed with the slow rates documented in the fossils, that one trait required a rate reduction (stabilizing selection), and the other faster rates (divergent selection). The combined paleontological and comparative approach taken here allows recognition that morphological stasis can be the dominant evolutionary pattern within species lineages, even in very young and radiating clades.

Disjunct distributions of freshwater snails testify to a central role of the Congo system in shaping biogeographical patterns in Africa.

BackgroundThe formation of the East African Rift System has decisively influenced the distribution and evolution of tropical Africa’s biota by altering climate conditions, by creating basins for large long-lived lakes, and by affecting the catchment and drainage directions of river systems. However, it remains unclear how rifting affected the biogeographical patterns of freshwater biota through time on a continental scale, which is further complicated by the scarcity of molecular data from the largest African river system, the Congo.ResultsWe study these biogeographical patterns using a fossil-calibrated multi-locus phylogeny of the gastropod family Viviparidae. This group allows reconstructing drainage patterns exceptionally well because it disperses very poorly in the absence of existing freshwater connections. Our phylogeny covers localities from major drainage basins of tropical Africa and reveals highly disjunct sister-group relationships between (a) the endemic viviparids of Lake Malawi and populations from the Middle Congo as well as between (b) the Victoria region and the Okavango/Upper Zambezi area.ConclusionsThe current study testifies to repeated disruptions of the distribution of the Viviparidae during the formation of the East African Rift System, and to a central role of the Congo River system for the distribution of the continent’s freshwater fauna during the late Cenozoic. By integrating our results with previous findings on palaeohydrographical connections, we provide a spatially and temporarily explicit model of historical freshwater biogeography in tropical Africa. Finally, we review similarities and differences in patterns of vertebrate and invertebrate dispersal. Amongst others we argue that the closest relatives of present day viviparids in Lake Malawi are living in the Middle Congo River, thus shedding new light on the origin of the endemic fauna of this rift lake.

Palaeobiology and evolution of the Late Cenozoic freshwater molluscs of the Turkana Basin: Iridinidae Swainson, 1840 and Etheriidae Deshayes, 1830 (Bivalvia: Etherioidea)

The palaeobiology of the Late Cenozoic freshwater molluscs that inhabited the Omo-Turkana Basin, situated in the eastern branch of the East African Rift System (Ethiopia, Kenya), remains poorly documented. Here we revise the taxonomy and palaeobiology of the bivalve superfamily Etherioidea from this region and discuss some palaeohydrological implications. In the Iridininae (Mutela, Pleiodon), the genus Iridina Lamarck, 1819 is revived for elongated iridinids with a denticulated hinge, since all fossil Iridininae of the Omo-Turkana Basin and most Miocene-Early Pleistocene Iridininae elsewhere in Africa have denticulate hinges that are not comparable to those of modern Mutela. In addition to the ubiquitous Etheria elliptica (Etheriidae), 11 iridinids are described, five of which are new to science, namely Chambardia feibeli, Iridina turkanica, I. omoensis, I. browni and Pleiodon bentoni. Most species do not show lacustrine adaptations and are/were part of a widespread East African fauna. This confirms the highly unstable character of the Pliocene-Holocene aquatic ecosystems in the Omo-Turkana Basin. Indications for intralacustrine speciation are only observed in the Late Pliocene-Early Pleistocene long-lived (similar to 250 ka or longer) Palaeolake Lorenyang. Williamsons (1981) evolutionary model for the Omo-Turkana Basin molluscs does not apply to the Etherioidea.Synopsis The palaeobiology of the Late Cenozoic freshwater molluscs that inhabited the Omo‐Turkana Basin, situated in the eastern branch of the East African Rift System (Ethiopia, Kenya), remains poorly documented. Here we revise the taxonomy and palaeobiology of the bivalve superfamily Etherioidea from this region and discuss some palaeohydrological implications. In the Iridininae (Mutela, Pleiodon), the genus Iridina Lamarck, 1819 is revived for elongated iridinids with a denticulated hinge, since all fossil Iridininae of the Omo‐Turkana Basin and most Miocene‐Early Pleistocene Iridininae elsewhere in Africa have denticulate hinges that are not comparable to those of modern Mutela. In addition to the ubiquitous Etheria elliptica (Etheriidae), 11 iridinids are described, five of which are new to science, namely Chambardia feibeli, Iridina turkanica, I. omoensis, I. browni and Pleiodon bentoni. Most species do not show lacustrine adaptations and are/were part of a widespread East African fauna. This confirms the highly unstable character of the Pliocene‐Holocene aquatic ecosystems in the Omo‐Turkana Basin. Indications for intralacustrine speciation are only observed in the Late Pliocene‐Early Pleistocene long‐lived (∼25o ka or longer) Palaeolake Lorenyang. Williamsons (1981) evolutionary model for the Omo‐Turkana Basin molluscs does not apply to the Etherioidea.

Growing population and ecosystem change increase human schistosomiasis around Lake Malaŵi

Multiple anthropogenic environmental stressors with reinforcing effects to the deterioration of ecosystem stability can obscure links between ecosystem change and the prevalence of infectious diseases. Incomplete understanding may lead to ineffective public health and disease control strategies, as appears to be the case with increased urogenital schistosomiasis in humans around Lake Malaŵi over recent decades. Sedimentation and eutrophication help explain historical changes in intermediate host range and parasite transmission. Hence, control strategies should account for abiotic changes.

Recurrent camouflaged invasions and dispersal of an Asian freshwater gastropod in tropical Africa

BackgroundNon-indigenous taxa currently represent a large fraction of the species and biomass of freshwater ecosystems. The accumulation of invasive taxa in combination with other stressors in these ecosystems may alter the habitats to which native taxa are adapted, which could elicit evolutionary changes in native populations and their ecological interactions. Assessing ecological and evolutionary consequences of invasions simultaneously may therefore be the most effective approach to study taxa with complex invasion histories. Here we apply such an integrated approach to the cerithioid gastropod Melanoides tuberculata, a model system in invasion biology.ResultsMolecular phylogenetics and ancestral range reconstructions allowed us to identify several independent Asian invasions in Lakes Malawi and Tanganyika, the Congo River, Nigeria and Cameroon. Some invasive M. tuberculata populations display much variation in shell morphology, and overlap in morphospace with M. tuberculata populations native to Africa. Experiments confirmed great ecophenotyic plasticity in some invasive populations, which, in combination with the overlap in disparity with native populations, masks invaders and their dispersal through Africa. Finally, the results of geographic modeling indicate that cryptic M. tuberculata invasions occurred primarily in densely populated areas.ConclusionsWe reveal the continental nature of invasions of Asian M. tuberculata to Africa. Several of the affected ecosystems have high endemicity in Cerithioidea: Lake Tanganyika has an unparalleled diversity in freshwater cerithioids (>10 endemic genera) and the Congo Basin and Lake Malawi are home to the two largest endemic species clusters of Melanoides in Africa (~12 and ~8 species, respectively). Cerithioids perform ecologically important functions in the benthic ecosystems of African freshwaters, but invaders and ecosystem change pose risks to their native diversity. We draw suggestions for more effective conservation strategies from our integrated approach.

Ecosystem change and establishment of an invasive snail alter gastropod communities in long-lived Lake Malawi

Biotic invasions can have far-reaching effects in isolated, eco-insular systems such as the African Great Lakes, certainly in synergy with other anthropogenic stressors that affect ecosystem stability. Interactions between invasive and indigenous taxa across trophic levels often tend to propagate throughout the ecosystem, but also those at the same trophic level may affect biodiversity. Here, we examine faunal interactions between an invasive Asian morph of the cerithioidean gastropod Melanoides tuberculata and indigenous gastropods in long-lived Lake Malawi. Studying quantitative samples, we document a negative spatial correlation between the established invader and endemic Melanoides species, and positive ones between invasive and native M. tuberculata, and between native Melanoides and schistosome-transmitting Bulinus. Comparison of modern and fossil samples indicates that Melanoides communities have changed since the middle Holocene from consisting predominantly of endemic taxa (~95%) toward a dominance by non-endemics (~80%). External evidence suggests that ecosystem change, such as increased sedimentation and eutrophication, and interactions between the invasive and endemic Melanoides species are the most likely causes for these changes. More in-depth study of the benthic ecosystem is required to document interaction mechanisms better, but the invasive taxon is playing an important role in reshaping communities and diversity in Lake Malawi.