Shared and unique patterns of embryo development in extremophile poeciliids

Background: Closely related lineages of livebearing fishes have independently adapted to two extreme environmental factors: toxic hydrogen sulphide (H2S) and perpetual darkness. Previous work has demonstrated in adult specimens that fish from these extreme habitats convergently evolved drastically increased head and offspring size, while cave fish are further characterized by reduced pigmentation and eye size. Here, we traced the development of these (and other) divergent traits in embryos of Poecilia mexicana from benign surface habitats (“surface mollies”) and a sulphidic cave (“cave mollies”), as well as in embryos of the sister taxon, Poecilia sulphuraria from a sulphidic surface spring (“sulphur mollies”). We asked at which points during development changes in the timing of the involved processes (i.e., heterochrony) would be detectible. Methods and Results: Data were extracted from digital photographs taken of representative embryos for each stage of development and each type of molly. Embryo mass decreased in convergent fashion, but we found patterns of embryonic fat content and ovum/embryo diameter to be divergent among all three types of mollies. The intensity of yellow colouration of the yolk (a proxy for carotenoid content) was significantly lower in cave mollies throughout development. Moreover, while relative head size decreased through development in surface mollies, it increased in both types of extremophile mollies, and eye growth was arrested in mid-stage embryos of cave mollies but not in surface or sulphur mollies. Conclusion: Our results clearly demonstrate that even among sister taxa convergence in phenotypic traits is not always achieved by the same processes during embryo development. Furthermore, teleost development is crucially dependent on sufficient carotenoid stores in the yolk, and so we discuss how the apparent ability of cave mollies to overcome this carotenoid-dependency may represent another potential mechanism explaining the lack of gene flow between surface and cave mollies

The existence of species rests on a metastable equilibrium between inbreeding and outbreeding

Background: Speciation corresponds to the progressive establishment of reproductive barriers between groups of individuals derived from an ancestral stock. Since Darwin did not believe that reproductive barriers could be selected for, he proposed that most events of speciation would occur through a process of separation and divergence, and this point of view is still shared by most evolutionary biologists today. 

Results: I do, however, contend that, if so much speciation occurs, it must result from a process of natural selection, whereby it is advantageous for individuals to reproduce preferentially within a group and reduce their breeding with the rest of the population, leading to a model whereby new species arise not by populations splitting into separate branches, but by small inbreeding groups “budding” from an ancestral stock. This would be driven by several advantages of inbreeding, and mainly by advantageous recessive phenotypes, which could only be retained in the context of inbreeding. Reproductive barriers would thus not arise passively as a consequence of drift in isolated populations, but under the selective pressure of ancestral stocks. Most documented cases of speciation in natural populations appear to fit the model proposed, with more speciation occurring in populations with high inbreeding coefficients, many recessive characters identified as central to the phenomenon of speciation, with these recessive mutations expected to be surrounded by patterns of limited genomic diversity.

Conclusions: Whilst adaptive evolution would correspond to gains of function that would, most of the time, be dominant, the phenomenon of speciation would thus be driven by mutations resulting in the advantageous loss of certain functions since recessive mutations very often correspond to the inactivation of a gene. A very important further advantage of inbreeding is that it reduces the accumulation of recessive mutations in genomes. A consequence of the model proposed is that the existence of species would correspond to a metastable equilibrium between inbreeding and outbreeding, with excessive inbreeding promoting speciation, and excessive outbreeding resulting in irreversible accumulation of recessive mutations that could ultimately only lead to the extinction.
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On the close relationship between speciation, inbreeding and recessive mutations.

Whilst the principle of adaptive evolution is unanimously recognised as being caused by the process of natural selection favouring the survival and/or reproduction of individuals having acquired new advantageous traits, a consensus has proven much harder to find regarding the actual origin of species. Indeed, since speciation corresponds to the establishment of reproductive barriers, it is difficult to see how it could bring a selective advantage because it amounts to a restriction in the opportunities to breed with as many and/or as diverse partners as possible. In this regard, Darwin himself did not believe that reproductive barriers could be selected for, and today most evolutionary biologists still believe that speciation can only occur through a process of separation allowing two populations to diverge sufficiently to become infertile with one another. I do, however, take the view that, if so much speciation has occurred, and still occurs around us, it cannot be a consequence of passive drift but must result from a selection process, whereby it is advantageous for groups of individuals to reproduce preferentially with one another and reduce their breeding with the rest of the population. 

In this essay, I propose a model whereby new species arise by “budding” from an ancestral stock, via a process of inbreeding among small numbers of individuals, driven by the occurrence of advantageous recessive mutations. Since the phenotypes associated to such mutations can only be retained in the context of inbreeding, it is the pressure of the ancestral stock which will promote additional reproductive barriers, and ultimately result in complete separation of a new species. I thus contend that the phenomenon of speciation would be driven by mutations resulting in the advantageous loss of certain functions, whilst adaptive evolution would correspond to gains of function that would, most of the time be dominant.

A very important further advantage of inbreeding is that it reduces the accumulation of recessive mutations in genomes. A consequence of the model proposed is that the existence of species would correspond to a metastable equilibrium between inbreeding and outbreeding, with excessive inbreeding promoting speciation, and excessive outbreeding resulting in irreversible accumulation of recessive mutations that could ultimately only lead to the species extinction. 
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Evolutionary biology for the 21st century

New theoretical and conceptual frameworks are required for evolutionary biology to capitalize on the wealth of data now becoming available from the study of genomes, phenotypes, and organisms - including humans - in their natural environments.Molecular and Cellular BiologyOrganismic and Evolutionary Biolog

A New Mechanism for Recurrent Adaptive Radiations

Models of adaptive radiation through intraspecific competition have attracted mounting attention. Here we show how extending such models in a simple manner, by including a quantitative trait under weak directional selection, naturally leads to rich macroevolutionary patterns involving recurrent adaptive radiations and extinctions. Extensive tests demonstrate the robustness of this finding to a wide range of variations in model assumptions. In particular, recurrent adaptive radiations and extinctions readily unfold both for asexual and for sexual populations. Since the mechanisms driving the investigated processes of endogenous diversification result from generic geometric features of the underlying fitness landscapes - frequency-dependent disruptive selection in one trait and weak directional selection in another - the reported phenomena can be expected to occur in a wide variety of eco-evolutionary settings

Essay: On the close relationship between speciation, inbreeding and recessive mutations.

Whilst the principle of adaptive evolution is unanimously recognised as being caused by the process of natural selection favouring the survival and/or reproduction of individuals having acquired new advantageous traits, a consensus has proven much harder to find regarding the actual origin of species. Indeed, since speciation corresponds to the establishment of reproductive barriers, it is difficult to see how it could bring a selective advantage because it amounts to a restriction in the opportunities to breed with as many and/or as diverse partners as possible. In this regard, Darwin himself did not believe that reproductive barriers could be selected for, and today most evolutionary biologists still believe that speciation can only occur through a process of separation allowing two populations to diverge sufficiently to become infertile with one another. I do, however, take the view that, if so much speciation has occurred, and still occurs around us, it cannot be a consequence of passive drift but must result from a selection process, whereby it is advantageous for groups of individuals to reproduce preferentially with one another and reduce their breeding with the rest of the population. 
In this essay, I propose a model whereby new species arise by “budding” from an ancestral stock, via a process of inbreeding among small numbers of individuals, driven by the occurrence of advantageous recessive mutations. Since the phenotypes associated to such mutations can only be retained in the context of inbreeding, it is the pressure of the ancestral stock which will promote additional reproductive barriers, and ultimately result in complete separation of a new species. I thus contend that the phenomenon of speciation would be driven by mutations resulting in the advantageous loss of certain functions, whilst adaptive evolution would correspond to gains of function that would, most of the time be dominant.
A very important further advantage of inbreeding is that it reduces the accumulation of recessive mutations in genomes. A consequence of the model proposed is that the existence of species would correspond to a metastable equilibrium between inbreeding and outbreeding, with excessive inbreeding promoting speciation, and excessive outbreeding resulting in irreversible accumulation of recessive mutations that could ultimately only lead to the species extinction. 
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Why Are There So Many Cichlid Species? On the Interplay of Speciation and Adaptive Radiation

The explosive speciation of cichlid fishes in the African great lakes has intrigued biologists for many decades. Interest was revitalized in 1996 after the publication in Science of geological data [1] indicating that the youngest lake, Lake Victoria, must have been completely dry during the most recent Ice perhaps as recently as 12,400 years ago. This implies that the approximately 500 haplochromine cichlid species must have evolved within this extremely short timespan from a single ancestral species [2]. But even with lower estimates of species number and higher estimates of the age of the species flock, the haplochromine cichlids still present one of the most dramatic examples of speciation and diversification in vertebrates

Predicting evolution and visualizing high-dimensional fitness landscapes

The tempo and mode of an adaptive process is strongly determined by the structure of the fitness landscape that underlies it. In order to be able to predict evolutionary outcomes (even on the short term), we must know more about the nature of realistic fitness landscapes than we do today. For example, in order to know whether evolution is predominantly taking paths that move upwards in fitness and along neutral ridges, or else entails a significant number of valley crossings, we need to be able to visualize these landscapes: we must determine whether there are peaks in the landscape, where these peaks are located with respect to one another, and whether evolutionary paths can connect them. This is a difficult task because genetic fitness landscapes (as opposed to those based on traits) are high-dimensional, and tools for visualizing such landscapes are lacking. In this contribution, we focus on the predictability of evolution on rugged genetic fitness landscapes, and determine that peaks in such landscapes are highly clustered: high peaks are predominantly close to other high peaks. As a consequence, the valleys separating such peaks are shallow and narrow, such that evolutionary trajectories towards the highest peak in the landscape can be achieved via a series of valley crossingsComment: 12 pages, 7 figures. To appear in "Recent Advances in the Theory and Application of Fitness Landscapes" (A. Engelbrecht and H. Richter, eds.). Springer Series in Emergence, Complexity, and Computation, 201