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Evolution of the uniquely adaptable lentiviral envelope in a natural reservoir host.

BACKGROUND: The ability of emerging pathogens to infect new species is likely related to the diversity of pathogen variants present in existing reservoirs and their degree of genomic plasticity, which determines their ability to adapt to new environments. Certain simian immunodeficiency viruses (SIVcpz, SIVsm) have demonstrated tremendous success in infecting new species, including humans, resulting in the HIV-1 and HIV-2 epidemics. Although SIV diversification has been studied on a population level, the essential substrates for cross-species transmission, namely SIV sequence diversity and the types and extent of viral diversification present in individual reservoir animals have not been elucidated. To characterize this intra-host SIV diversity, we performed sequence analyses of clonal viral envelope (env) V1V2 and gag p27 variants present in individual SIVsm-infected sooty mangabeys over time. RESULTS: SIVsm demonstrated extensive intra-animal V1V2 length variation and amino acid diversity (le38%), and continual variation in V1V2 N-linked glycosylation consensus sequence frequency and location. Positive selection was the predominant evolutionary force. Temporal sequence shifts suggested continual selection, likely due to evolving antibody responses. In contrast, gag p27 was predominantly under purifying selection. SIVsm V1V2 sequence diversification is at least as great as that in HIV-1 infected humans, indicating that extensive viral diversification in and of itself does not inevitably lead to AIDS. CONCLUSION: Positive diversifying selection in this natural reservoir host is the engine that has driven the evolution of the uniquely adaptable SIV/HIV envelope protein. These studies emphasize the importance of retroviral diversification within individual host reservoir animals as a critical substrate in facilitating cross-species transmission.

Animals↗

To diversify or not to diversify.

One of the most challenging decisions a company can confront is whether to diversify. The rewards and risks are extraordinary. Success stories such as General Electric, Disney, and 3M abound, but so do stories of failure-consider Quaker Oats' entry into the fruit juice business with Snapple. What makes diversification such an unpredictable, high-stakes game? First, companies usually face the decision in an atmosphere that is not conducive to thoughtful deliberation. For example, an attractive company comes into play, and a competitor is interested in buying it. Or the board of directors urges expanding into new markets. Suddenly, senior managers must synthesize mountains of data under intense time pressure. To complicate matters, diversification as a corporate strategy regularly goes in and out of vogue. In short, there is little conventional wisdom to guide managers as they consider a move that could greatly increase shareholder value or seriously damage it. But diversification doesn't need to be quite such a roll of the dice, argues the author. His research suggests that if managers consider six questions, they can reduce the gamble of diversification. Answering the questions will not lead to an easy go-no-go decision, but by helping managers weigh risks and opportunities, it can help them assess the likelihood of success. The issues that the questions raise, and the discussion they provoke, are meant to be coupled with the detailed financial analysis usually conducted before a diversification decision is made. Together, these tools can turn a complex and often pressured decision into a more structured and well-reasoned one.

Commerce↗

Transposable Element-Mediated Cis-Regulation Drives the Evolution of dmrt1 as a Candidate Master Sex-Determining Gene in Black Carp.

Sex determination in vertebrates exhibits remarkable evolutionary plasticity, with diverse mechanisms and master sex-determining (MSD) genes arising independently across lineages. Among these, dmrt1, a dosage-sensitive gene, has repeatedly been recruited as an MSD gene through gene duplication or allelic diversification. However, the biochemical basis of such evolutionary transitions, particularly those driven by allelic diversification, remains largely unexplored. Here, we generated haplotype-resolved genome assemblies for both XX and XY black carp (Mylopharyngodon piceus) and identified a ∼40-kb region on chromosome 4, containing only dmrt1, as the candidate sex-determining locus. We discovered two Y-specific insertions in the dmrt1 promoter: a 13.4-kb highly repetitive element and an 11-bp motif. Functional assays revealed that these insertions act as enhancer and a promoter element, respectively, driving early, allele-specific upregulation of dmrt1 prior to gonadal differentiation. Notably, the 13.4-kb insertion contains transposable elements (TEs) functioning as cis-regulatory modules with transcription factor binding sites that mediate Y-specific activation. Our findings reveal a TE-mediated regulatory innovation that promoted dmrt1's evolution as a male-determining gene via allelic diversification, providing new insights into how mobile genetic elements drive the origin and diversification of sex-determining systems in vertebrates.

Animals↗

Phylogeographic structure in the bogus yucca moth Prodoxus quinquepunctellus (Prodoxidae): comparisons with coexisting pollinator yucca moths.

The pollination mutualism between yucca moths and yuccas highlights the potential importance of host plant specificity in insect diversification. Historically, one pollinator moth species, Tegeticula yuccasella, was believed to pollinate most yuccas. Recent phylogenetic studies have revealed that it is a complex of at least 13 distinct species, eight of which are specific to one yucca species. Moths in the closely related genus Prodoxus also specialize on yuccas, but they do not pollinate and their larvae feed on different plant parts. Previous research demonstrated that the geographically widespread Prodoxus quinquepunctellus can rapidly specialize to its host plants and may harbor hidden species diversity. We examined the phylogeographic structure of P. quinquepunctellus across its range to compare patterns of diversification with six coexisting pollinator yucca moth species. Morphometric and mtDNA cytochrome oxidase I sequence data indicated that P. quinquepunctellus as currently described contains two species. There was a deep division between moth populations in the eastern and the western United States, with limited sympatry in central Texas; these clades are considered separate species and are redescribed as P. decipiens and P. quinquepunctellus (sensu stricto), respectively. Sequence data also showed a lesser division within P. quinquepunctellus s.s. between the western populations on the Colorado Plateau and those elsewhere. The divergence among the three emerging lineages corresponded with major biogeographic provinces, whereas AMOVA indicated that host plant specialization has been relatively unimportant in diversification. In comparison, the six pollinator species comprise three lineages, one eastern and two western. A pollinator species endemic to the Colorado Plateau has evolved in both of the western lineages. The east-west division and the separate evolution of two Colorado Plateau pollinator species suggest that similar biogeographic factors have influenced diversification in both Tegeticula and Prodoxus. For the pollinators, however, each lineage has produced a monophagous species, a pattern not seen in P. quinquepunctellus.

Analysis of Variance↗

Slow myosins in muscle development.

Myogenesis has been a system central to investigations on mechanisms of diversification within groups of differentiating cells. Diversity among cell types has been well described in striated muscle tissue at the protein and enzymatic-function levels for decades, but it is only in recent years that some understanding of the molecular mechanisms responsible for this diversity has begun to emerge. Study of the expression of the slow isoforms of the myosin heavy chain has contributed to our understanding of how cell diversity arises within skeletal and cardiac muscle. Slow MyHc isoforms are developmentally responsive to a number of cues provided by the nervous systems, the endocrine system and, later in development, to functional demands on these developing tissues. Perhaps most informative have been studies on the mechanism for regulation of slow MyHc expression in mammals and birds where studies on the calcineurin-NF-AT pathways and nuclear hormone action have been shown to control MyHC gene expression in skeletal muscle and in the developing heart. The mechanisms involved in cell diversification in myogenesis are undoubtedly more varied and complex than those currently offered to explain cell diversification, but these recent studies have broadened our understanding of the interplay between the nervous system, the endocrine system and cell lineages in controlling cell diversification. Greater focus on the first fibers and cardiomyocytes to form in the embryo are likely to bring additional insights into the mechanism crucial for establishing the patterns of diversity required for successful formation of embryonic tissues.

Animals↗

Diversity in times of adversity: probabilistic strategies in microbial survival games.

Population diversification strategies are ubiquitous among microbes, encompassing random phase-variation (RPV) of pathogenic bacteria, viral latency as observed in some bacteriophage and HIV, and the non-genetic diversity of bacterial stress responses. Precise conditions under which these diversification strategies confer an advantage have not been well defined. We develop a model of population growth conditioned on dynamical environmental and cellular states. Transitions among cellular states, in turn, may be biased by possibly noisy readings of the environment from cellular sensors. For various types of environmental dynamics and cellular sensor capability, we apply game-theoretic analysis to derive the evolutionarily stable strategy (ESS) for an organism and determine when that strategy is diversification. We find that: (1) RPV, effecting a sort of Parrondo paradox wherein random alternations between losing strategies produce a winning strategy, is selected when transitions between different selective environments cannot be sensed, (2) optimal RPV cell switching rates are a function of environmental lifecycle asymmetries and environmental autocorrelation, (3) probabilistic diversification upon entering a new environment is selected when sensors can detect environmental transitions but have poor precision in identifying new environments, and (4) in the presence of excess additive noise, low-pass filtering is required for evolutionary stability. We show that even when RPV is not the ESS, it may minimize growth rate variance and the risk of extinction due to 'unlucky' environmental dynamics.

Bacteria↗

Modifiers of muscle and heart cell fate specification identified by gain-of-function screen in Drosophila.

The homeobox genes ladybird in Drosophila and their vertebrate counterparts Lbx1 genes display restricted expression patterns in a subset of muscle precursors and are both implicated in diversification of muscle cell fates. In order to gain new insights into mechanisms controlling conserved aspects of cell fate specification, we have performed a gain-of-function (GOF) screen for modifiers of the mesodermal expression of ladybird genes using a collection of EP element carrying Drosophila lines. Amongst the identified genes, several have been previously implicated in cell fate specification processes, thus validating the strategy of our screen. Observed GOF phenotypes have led us to identification of an important number of candidate genes, whose myogenic and/or cardiogenic functions remain to be investigated. Amongst them, the EP insertions close to rhomboid, yan and rac2 suggest new roles for these genes in diversification of muscle and/or heart cell lineages. The analysis of loss and GOF of rhomboid and yan reveals their new roles in specification of ladybird-expressing precursors of adult muscles (LaPs) and ladybird/tinman-positive pericardial cells. Observed phenotypes strongly suggest that rhomboid and yan act at the level of progenitor and founder cells and contribute to the diversification of mesodermal fates. Our analysis of rac2 phenotypes clearly demonstrates that the altered mesodermal level of Rho-GTPase Rac2 can influence specification of a number of cardiac and muscular cell types including those expressing ladybird. Finding that in rac2 mutants ladybird and even skipped-positive muscle founders are overproduced, indicate a new early function for this gene during segregation of muscle progenitors and/or specification of founder cells. Intriguingly, rhomboid, yan and rac2 act as conserved components of Receptor Tyrosine Kinases (RTKs) signalling pathways, suggesting that RTK signalling constitutes a part of a conserved regulatory network governing diversification of muscle and heart cell types.

Animals↗

A critical reappraisal of the fossil record of the bilaterian phyla.

It has long been assumed that the extant bilaterian phyla generally have their origin in the Cambrian explosion, when they appear in an essentially modern form. Both these assumptions are questionable. A strict application of stem- and crown-group concepts to phyla shows that although the branching points of many clades may have occurred in the Early Cambrian or before, the appearance of the modern body plans was in most cases later: very few bilaterian phyla sensu stricto have demonstrable representatives in the earliest Cambrian. Given that the early branching points of major clades is an inevitable result of the geometry of clade diversification, the alleged phenomenon of phyla appearing early and remaining morphologically static is seen not to require particular explanation. Confusion in the definition of a phylum has thus led to attempts to explain (especially from a developmental perspective) a feature that is partly inevitable, partly illusory. We critically discuss models for Proterozoic diversification based on small body size, limited developmental capacity and poor preservation and cryptic habits, and show that the prospect of lineage diversification occurring early in the Proterozoic can be seen to be unlikely on grounds of both parsimony and functional morphology. Indeed, the combination of the body and trace fossil record demonstrates a progressive diversification through the end of the Proterozoic well into the Cambrian and beyond, a picture consistent with body plans being assembled during this time. Body-plan characters are likely to have been acquired monophyletically in the history of the bilaterians, and a model explaining the diversity in just one of them, the coelom, is presented. This analysis points to the requirement for a careful application of systematic methodology before explanations are sought for alleged patterns of constraint and flexibility.

Animals↗

Differential expression patterns of the hox gene are associated with differential growth of insect hind legs.

Diversification of leg appendages is one of the hallmarks of morphological evolution in insects. In particular, insect hind (T3) legs exhibit a whole spectrum of morphological diversification, ranging from uniform to extremely modified. To elucidate the developmental basis of T3 leg evolution, we have examined the expression patterns of two homeotic genes, Ultrabithorax and abdominal-A (collectively referred to as UbdA), in a broad range of species. First, our results show that UbdA expression in hemimetabolous insects is localized only in specific T3 leg segments undergoing differential growth (compared to their foreleg counterparts). In contrast, in basal hexapod and insect lineages, the absence of the UbdA signal coincides with uniform leg morphology. The same situation exists in first instar larvae of holometabolous insects, in which absence of UbdA expression in the embryonic T3 legs is associated with the lack of larval T3 leg diversification. Second, there is a clear difference in the timing of expression between species with greatly enlarged T3 leg, such as crickets and grasshoppers, and species that exhibit more moderate enlargement of hind legs, such as mantids and cockroaches. In the former, the UbdA expression starts much earlier, coinciding with the elongation of T3 limb buds. In the latter, however, the UbdA expression starts at much later stages of development, coinciding with the establishment of distinct leg segments. These results suggest that diversification of insect hind legs was influenced by changes in both the spatial and temporal regulation of the UbdA expression.

Animals↗

Convergent evolution of behavior in an adaptive radiation of Hawaiian web-building spiders.

Species in ecologically similar habitats often display patterns of divergence that are strikingly comparable, suggesting that natural selection can lead to predictable evolutionary change in communities. However, the relative importance of selection as an agent mediating in situ diversification, versus dispersal between habitats, cannot be addressed without knowledge of phylogenetic history. We used an adaptive radiation of spiders within the Hawaiian Islands to test the prediction that species of spiders on different islands would independently evolve webs with similar architectures. Tetragnatha spiders are the only nocturnal orb-weaving spiders endemic to the Hawaiian archipelago, and multiple species of orb-weaving Tetragnatha co-occur within mesic and wet forest habitats on each of the main islands. Therefore, comparison of web architectures spun by spiders on different islands allowed study of replicated evolutionary events of past behavioral diversification. We found that species within each island construct webs with architectures that differ from one another. However, pairs of species on different islands, "ethotypes," share remarkable similarities in web architectures. Phylogenetic analysis demonstrated that the species comprising these ethotypes evolved independent of one another. Our study illustrates the high degree of predictability that can be exhibited by the evolutionary diversification of complex behaviors. However, not all web architectures were shared between islands, demonstrating that unique effects also have played an important role in the historical diversification of behavior.

Adaptation, Physiological↗

Lessons from the past: evolutionary impacts of mass extinctions.

Mass extinctions have played many evolutionary roles, involving differential survivorship or selectivity of taxa and traits, the disruption or preservation of evolutionary trends and ecosystem organization, and the promotion of taxonomic and morphological diversifications-often along unexpected trajectories-after the destruction or marginalization of once-dominant clades. The fossil record suggests that survivorship during mass extinctions is not strictly random, but it often fails to coincide with factors promoting survival during times of low extinction intensity. Although of very serious concern, present-day extinctions have not yet achieved the intensities seen in the Big Five mass extinctions of the geologic past, which each removed > or =50% of the subset of relatively abundant marine invertebrate genera. The best comparisons for predictive purposes therefore will involve factors such as differential extinction intensities among regions, clades, and functional groups, rules governing postextinction biotic interchanges and evolutionary dynamics, and analyses of the factors that cause taxa and evolutionary trends to continue unabated, to suffer setbacks but resume along the same trajectory, to survive only to fall into a marginal role or disappear ("dead clade walking"), or to undergo a burst of diversification. These issues need to be addressed in a spatially explicit framework, because the fossil record suggests regional differences in postextinction diversification dynamics and biotic interchanges. Postextinction diversifications lag far behind the initial taxonomic and morphological impoverishment and homogenization; they do not simply reoccupy vacated adaptive peaks, but explore opportunities as opened and constrained by intrinsic biotic factors and the ecological and evolutionary context of the radiation.

Animals↗

Documenting a significant relationship between macroevolutionary origination rates and Phanerozoic pCO2 levels.

We show that the rates of diversification of the marine fauna and the levels of atmospheric CO(2) have been closely correlated for the past 545 million years. These results, using two of the fundamental databases of the Earth's biota and the Earth's atmospheric composition, respectively, are highly statistically significant (P < 0.001). The strength of the correlation suggests that one or more environmental variables controlling CO(2) levels have had a profound impact on evolution throughout the history of metazoan life. Comparing our work with highly significant correlations described by D. H. Rothman [Rothman, D. H. (2001) Proc. Natl. Acad. Sci. USA 98, 4305-4310] between total biological diversity and a measure of stable carbon isotope fractionation, we find that the rates of diversification rather than total diversification correlate with environmental variables, and that the rate of diversification follows the record of CO(2) projected by R. A. Berner and Z. Kothavala [Berner, R. A. & Kothavala, Z. (2001) Am. J. Sci. 301, 182-204] more closely than that predicted by Rothman.

Biological Evolution↗

Why do species exist? Insights from sexuals and asexuals.

Why does life diversify into the more or less discrete entities we recognise as species? Two main explanations have been proposed: i) species are a consequence of adaptation to different ecological niches, ii) species are a consequence of sexual reproduction and reproductive isolation. Phylogenetic studies of case-study groups can provide insights into the relative importance of divergent selection and isolation for speciation, but it can be difficult to infer causes of speciation unambiguously. The example of North American tiger beetles from the genus Cicindela is discussed. An alternative approach is to compare diversification between related sexual and asexual taxa to infer the relative importance of the two explanations. We outline expected patterns of diversification in sexual and asexual lineages under different scenarios using coalescent theory. Whether sexuals or asexuals diversify to a greater extent depends on the balance among various stages of diversification, particularly on the effects of sexual reproduction on rates of adaptive evolution. Rotifers offer a unique system to test these ideas, allowing comparison of patterns of genetic and functional morphological diversification in sexual (bdelloid) and asexual (monogonont) clades.

Journal Article↗

Taxonomic level as a determinant of the shape of the Phanerozoic marine biodiversity curve.

Key aims of recent paleobiological research have been the construction of Phanerozoic global biodiversity patterns and the formulation of models and mechanisms of diversification describing such patterns. Two conflicting theories of global diversification have been equilibrium versus expansionist growth of taxonomic diversity. These models, however, rely on accurate empirical data curves, and it is not clear to what extent the taxonomic level at which the data are analyzed controls the resulting pattern. Global Phanerozoic marine diversity curves are constructed at ordinal, familial, and generic levels using several fossil-range data sets. The fit of a single logistic model reduces from ordinal through familial to generic level, while conversely, that of an exponential growth model increases. Three sequential logistic equations, fitted to three time periods during which diversity appears to approach or reach an equilibrium state, provide the best description of the data at familial and generic levels. However, an exponential growth curve describes the diversification of marine life since the end-Permian extinction equally as well as a logistic. A species-level model of global Phanerozoic marine diversification, constructed by extrapolation of the trends from familial to generic level, suggests growth in numbers of marine species was broadly exponential. When smaller subsets of the data are analyzed, the effect of taxonomic level on the shape of the diversity curve becomes more pronounced. In the absence of species data, a consistent signal at more than one higher taxonomic level is required to predict a species-level pattern.

Ecosystem↗

Molecular phylogeny, recent radiation and evolution of gross morphology of the rhubarb genus Rheum (Polygonaceae) inferred from chloroplast DNA trnL-F sequences.

BACKGROUND AND AIMS: Rheum, a highly diversified genus with about 60 species, is mainly confined to the mountainous and desert regions of the Qinghai-Tibetan plateau and adjacent areas. This genus represents a good example of the extensive diversification of the temperate genera in the Qinghai-Tibetan plateau, in which the forces to drive diversification remain unknown. To date, the infrageneric classification of Rheum has been mainly based on morphological characters. However, it may have been subject to convergent evolution under habitat pressure, and the systematic position of some sections are unclear, especially Sect. Globulosa, which has globular inflorescences, and Sect. Nobilia, which has semi-translucent bracts. Recent palynological research has found substantial contradictions between exine patterns and the current classification of Rheum. Two specific objectives of this research were (1) to evaluate possible relationships of some ambiguous sections with a unique morphology, and (2) to examine possible occurrence of the radiative speciation with low genetic divergence across the total genus and the correlation between the extensive diversification time of Rheum and past geographical events, especially the recent large-scale uplifts of the Qinghai-Tibetan Plateau. METHODS: The chloroplast DNA trnL-F region of 29 individuals representing 26 species of Rheum, belonging to seven out of eight sections, was sequenced and compared. The phylogenetic relationships were further constructed based on the sequences obtained. KEY RESULTS: Despite the highly diversified morphology, the genetic variation in this DNA fragment is relatively low. The molecular phylogeny is highly inconsistent with gross morphology, pollen exine patterns and traditional classifications, except for identifying all samples of Sect. Palmata, three species of Sect. Spiciformia and a few species of Sect. Rheum as corresponding monophyletic groups. The monotypic Sect. Globulosa showed a tentative position within the clade comprising five species of Sect. Rheum. All of the analyses revealed the paraphyly of R. nobile and R. alexandrae, the only two species of Sect. Nobilia circumscribed by the possession of large bracts. The crude calibration of lineages based on trnL-F sequence differentiation implied an extensive diversification of Rheum within approx. 7 million years. CONCLUSIONS: Based on these results, it is suggested that the rich geological and ecological diversity caused by the recent large-scale uplifts of the Qinghai-Tibetan Plateau since the late Tertiary, coupled with the oscillating climate of the Quaternary stage, might have promoted rapid speciation in small and isolated populations, as well as allowing the fixation of unique or rare morphological characters in Rheum. Such a rapid radiation, combined with introgressive hybridization and reticulate evolution, may have caused the transfer of cpDNA haplotypes between morphologically dissimilar species, and might account for the inconsistency between morphological classification and molecular phylogeny reported here.

Biological Evolution↗

Newspaper and wire service coverage of tobacco farmers.

This study examined print media coverage of tobacco farmers from the perspective of agenda setting, or the extent to which information is available to the public and perceived as important. A content analysis of 743 articles published between January 1, 1995 and June 30, 1997 was completed. The number of articles increased from 1995 to 1997. Of the topics analyzed, articles on tobacco settlement (7.1% of total) and diversification (15.6% of total) were the least prevalent. Because the settlement discussions did not occur until 1997 (when it comprised 26.4% of the total in the first 6 months), diversification was consistently the least covered topic. The two most frequent topics covered were tobacco companies (36.2%) and the tobacco price support program (32.3%). Except for one 6 month interval, there were substantially more articles in local/regional publications than in national publications. Public health professionals have called for tobacco farmers to diversify to non-tobacco enterprises. Yet, there is little discussion of diversification in print media. Without more attention to diversification, the public and policy makers will be ill-informed about opportunities and obstacles in this regard.

Agriculture↗

On the origin of the Synodontis catfish species flock from Lake Tanganyika.

Species flocks within Great Lakes provide unique insights into the factors affecting diversification. Lake Tanganyika (LT) is of particular interest because it contains many endemic groups for which general factors affecting diversification can be discerned. Here, we present the first phylogenetic study of the LT Synodontis (Siluriformes, Mochokidae) species flock using mtDNA sequence data. Our data reveal some previously unrecognized species diversity and indicate that the LT species flock is not monophyletic, and that two closely related clades of endemics may have independently colonized LT. Other comparable small species flocks are characterized by a single colonization event. Molecular date estimates of the timing of the initial within-lake diversification of the LT endemics, based on a fossil calibration, are comparable to those reported for other groups, suggesting that extrinsic factors maybe important common causes of clade diversification. The basal divergence in the sampled Synodontis reveals an East-West African faunal split seen in many terrestrial, but few aquatic groups, the timing of which coincides with East African rifting events.

Africa, Eastern↗

Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika.

Ancient lakes are often collectively viewed as evolutionary hot spots of diversification. East Africa's Lake Tanganyika has long been the subject of scientific interest owing to dramatic levels of endemism in species as diverse as cichlid fishes, paludomid gastropods, decapod and ostracod crustaceans and poriferans. It is the largest and deepest of the African rift lakes, and its endemic fauna has been presented with a stable inland environment for over 10 Myr, offering unique opportunities for within-lake diversification. Although astonishing diversification has been documented in the endemic cichlid fauna of the lake, similar patterns of rapid diversification have long been assumed for other groups. In contrast to this hypothesis of rapid speciation, we show here that there has been no acceleration in the rate of speciation in the thalassoid gastropods of the lake following lake colonization. While limited within-lake speciation has occurred, the dramatic conchological diversity of gastropods presently found within the lake has evolved from at least four major lineages that pre-date its formation by as much as 40 Myr. At the same time, a widespread group of African gastropods appears to have evolved from taxa presently found in the lake. While Lake Tanganyika has been a cradle of speciation for cichlid fishes, it has also been an important evolutionary reservoir of gastropod lineages that have been extirpated outside the basin.

Animals↗