Evolutionary Dead End Research Articles

Progenesis as an intrinsic factor of ecological opportunity in a polyphenic amphibian

Abstract Paedomorphosis, a developmental heterochrony involving the retention of larval traits at the adult stage, is considered a major evolutionary process because it can generate phenotypic variation without requiring genetic modifications. Two main processes underlie paedomorphosis: neoteny, a slowdown of somatic development, and progenesis, a precocious maturation associated with body size reduction. Being essentially a truncation of ontogeny, progenesis has often been deemed an evolutionary dead end with advantages attributed to precocious reproduction or small body size required in specific environmental contexts (e.g. parasitism, interstitial life), but there is a lack of studies on the immediate ecological consequences of progenesis. Because body size is a key factor determining trophic ecology in animals, we hypothesized that progenesis might intrinsically promote ecological opportunity via body size reduction (i.e. ‘the trophic advantage of progenesis’ hypothesis). We tested this hypothesis in facultatively progenetic palmate newts Lissotriton helveticus using stable isotope niche modelling and diet reconstruction in conjunction with traditional stomach content analyses and body condition (BC) assessment. We show that not only did progenetic individuals occupy a different trophic niche than metamorphic individuals in all populations, but the smaller they were compared to metamorphs due to progenesis, the more different they were in terms of trophic ecology, with no negative effect on their BC. Altogether, the results suggest that via body size reduction, progenesis may generally act as an intrinsic factor of ecological opportunity, allowing the use of existing but previously unavailable resources, even in habitats where seemingly little opportunity exists. We argue that beyond the classically recognized fitness advantages of progenetic development, this process may also generally bring an immediate trophic advantage via body size reduction, which would have important implications to understand the evolution and adaptiveness of this process in many different taxa, from marine meiofauna to primates. A free Plain Language Summary can be found within the Supporting Information of this article.

The correlation of phylogenetics, elevation and ploidy on the incidence of apomixis in Asteraceae in the European Alps

Abstract Asexual reproduction has often been regarded as an evolutionary dead end, but asexual lineages (most notably those that are apomictic) are present in several angiosperm families and often comprise a large number of taxa, both widespread and endemic. Investigating correlations between genetic, environmental and taxonomic factors and the incidence of apomixis has represented a challenge for many years, with previous analyses frequently omitting one or more of these variables. Here, flow cytometric seed screening, cytological data and ecological variables have been integrated in a phylogenetic framework to create a comprehensive dataset for 229 of Asteraceae from the European Alps. Data were analysed using phylogenetically informed generalized linear mixed models (pMCMCglmm) where elevation, ploidy and phenology were assessed for their potential correlation with asexual reproduction and apomixis type. Although apomixis is not dominant among the species studied, our results confirm that an odd ploidy (e.g. 3x) and, to a lesser extent, an even polyploid level (i.e. 4x) significantly increase its probability, most probably due to chromosome misalignments during meiosis. The distribution of apomictic species does not correlate with elevation, and there is a weak correlation between early flowering initiation and aposporous apomixis. Although current and future changes in climate may severely impact the survival of the flora of the European Alps, asexual reproduction and polyploidization may prove to be, at least temporarily, lifelines for the survival of a species under the novel climatic conditions. Therefore, uncovering how apomicts and polyploids evolve and persist will be essential for understanding the ecology of the European Alps and hence informing future conservation strategies.

Pilar Catalán.

Pilar Catalán.

Buzz pollination

Pritchard and Vallejo-Marín introduce the process and evolution of buzz pollination.

Diversity, Ecology, Biogeography, and Evolution of the Prevalent Brown Algal Genus Lobophora in the Greater Caribbean Sea, Including the Description of Five New Species1.

Distributed in tropical and warm-temperate waters worldwide, Lobophora species are found across the Greater Caribbean (i.e., Caribbean sensu stricto, Gulf of Mexico, Florida, the Bahamas, and Bermuda). We presently discuss the diversity, ecology, biogeography, and evolution of the Greater Caribbean Lobophora species based on previous studies and an extensive number of samples collected across the eastern, southern, and to a lesser extent western Caribbean. A total of 18 Lobophora species are now documented from the Greater Caribbean, of which five are newly described (L. agardhii sp. nov., L. dickiei sp. nov., L. lamourouxii sp. nov., L. richardii sp. nov., and L. setchellii sp. nov.). Within the Greater Caribbean, the eastern Caribbean and the Central Province are the most diverse ecoregion and province (16 spp.), respectively. Observed distribution patterns indicate that Lobophora species from the Greater Caribbean have climate affinities (i.e., warm-temperate vs. tropical affinities). In total, 11 Lobophora species exclusively occur in the Greater Caribbean; six are present in the western Atlantic; two in the Indo-Pacific; and one in the eastern Pacific. Biogeographic analyses support that no speciation occurred across the Isthmus of Panama, and that the Greater Caribbean acted as a recipient region for species from the Indo-Pacific and as a region of diversification as well as a donor region to the North-eastern Atlantic. The Greater Caribbean is not an evolutionary dead end for Lobophora, but instead generates and exports diversity. Present results illustrate how sampling based on DNA identification is reshaping biogeographic patterns, as we know them.

Placing the hybrid origin of the asexual Amazon molly (Poecilia formosa) based on historical climate data

Abstract Asexual hybrids are important model organisms for addressing questions in evolution and ecology, especially for understanding the role of hybridization in speciation. They are rare in nature and several hypotheses have been suggested to explain this. We use an asexual fish, the Amazon molly (Poecilia formosa), to establish the area in which it was formed via hybridization 125 000 years ago. Using species distribution models and climate models for the Last Interglacial (LIG) we found that model projections to the LIG show a similar map to the present climate model and parental species potentially overlapped in a relatively small area near Tampico, Mexico. This makes P. formosa one of a few hybrid species for which we know the parental species, the time of hybridization, and likely the place of hybridization. Based on the small area of overlap, our data is in agreement with the idea that asexual hybrids may be rare not because they are evolutionary dead ends but are formed rarely.

Substantially adaptive potential in polyploid cyprinid fishes: evidence from biogeographic, phylogenetic and genomic studies.

Whole genome duplication (WGD) is commonly believed to play key roles in vertebrate evolution. However, nowadays polyploidy exists in a few fish, amphibian and reptile groups only, and seems to be an evolutionary dead end in vertebrates. We investigate the evolutionary significance of polyploidization in Cyprinidae-a fish family that contains more polyploid species than any other vertebrate group-with integrated biogeographic, phylogenetic and genomic analyses. First, polyploid species are found to be significantly frequent in areas of higher altitude and lower mean annual temperature compared with diploid species in Cyprinidae. Second, a polyploidy-related diversification rate shift is observed in Cyprinidae. This increased net diversification rate is only seen in three polyploid lineages, and other polyploid lineages have similar net diversification rate as well as diploid lineages in Cyprinidae. Interestingly, significant 'lag times' existed between polyploidization and radiation in Cyprinidae. Multiple polyploid lineages were established approximately 15 Ma through recurrent allopolyploidization events, but the net diversification rate did not start to increase until approximately 5 Ma-long after polyploidization events. Environmental changes associated with the continuous uplift of the Tibetan Plateau and climate change have probably promoted the initial establishment and subsequent radiation of polyploidy in Cyprinidae. Finally, the unique retention of duplicated genes in polyploid cyprinids adapted to harsh environments is found. Taken together, our results suggest that polyploidy in Cyprinidae is far more than an evolutionary dead end, but rather shows substantially adaptive potential. Polyploid cyprinids thus constitute an ideal model system for unveiling largely unexplored consequences of WGD in vertebrates, from genomic evolution to species diversification.

Character expression, reproductive barriers, and origin of the rare fern hybrid Asplenium ×aran-tohanum (Aspleniaceae)

Hybridization is a ubiquitous force in plant evolution. In ferns, hybrids are often easily recognized by their intermediate morphology and abortive spores and thus provide a good model for studying reproductive isolating barriers between species. Asplenium ×aran-tohanum is a rare fern hybrid, despite wide coexistence of its parental species (A. billotii and A. trichomanes subsp. quadrivalens) in Western Europe. We made a complete characterization of its three known individuals, including macro- and micromorphology, sporogenesis, gametophyte reproduction, and chloroplast DNA inheritance and evolution. The hybrid expressed morphological characters that were mostly intermediate between those of the parents, but some characters were more similar to one parent or the other. Sizes of both guard cells and spores indicate that the hybrid is tetraploid, as are both parents, and one parent (A. billotii) consistently acted as the female. A very small fraction of spores (~ 7%) were viable and the resulting gametophytes could not form sporophytes, either sexually or apogamously, suggesting that effective postzygotic barriers exist between the parents. The lineages of these taxa diverged about 35 million years ago, which may explain the strong reproductive isolation and rarity of the hybrid. Asplenium ×aran-tohanum appears to be an evolutionary dead end, probably formed recurrently at the places where it grows, but incapable of completing its life cycle or producing viable offspring.

Ecomorphological specialization leads to loss of evolvability in primate limbs.

Primate limb morphology is often described as either generalized, that is, suited to a range of locomotor and positional behaviors, or specialized for unique locomotor behaviors such as brachiation or bipedalism. The evolution of highly specialized limb morphology may result in loss of evolvability, that is, in a decreased capacity of the locomotor skeleton to evolve in response to selection towards alternative ecomorphological niches. Using evolutionary simulations, I show that the highly specialized limb anatomy of hominoids is associated with a significant loss of evolvability, defined as the number of generations to reach alternative adaptive peaks, and in parallel an increased risk of extinction, particularly in simulated evolution toward generalized quadrupedal limb proportions. Loss of evolvability in apes and humans correlates with three factors: (1) decreased correlation among limb bone lengths (i.e., integration), which slows the rate of change along lines of least evolutionary resistance; (2) limb specialization, which places apes and humans in relatively remote areas of morphospace; and (3) increased skeletal size as a proxy for body size. Thus, locomotor over-specialization can lead to evolutionary dead-ends that significantly increase the probability of hominoid populations going extinct before evolving new adaptive morphologies.

Unisexual hybrids break through an evolutionary dead end by two-way backcrossing.

Unisexual vertebrates (i.e., those produced through clonal or hemiclonal reproduction) are typically incapable of purging deleterious mutations, and, as a result, are considered short-lived in evolutionary terms. In hemiclonal reproduction (hybridogenesis), one parental genome is eliminated during oogenesis, producing haploid eggs containing the genome of a single parent. Hemiclonal hybrids are usually produced by backcrossing hemiclonal hybrids with males of the paternal species. When hemiclonal hybrids from a genus of greenlings (Hexagrammos) are crossed with males of the maternal species, the progeny are phenotypically similar to the maternal species and produce recombinant gametes by regular meiosis. The present study was conducted to determine if the hemiclonal genome is returned to the gene pool of the maternal species in the wild. Using a specific cytogenetic marker to discriminate between such progeny and the maternal species, we observed that Hexagrammos hybrids mated with maternal and paternal ancestors at the same frequency. This two-way backcrossing in which clonal genomes are returned to the gene pool where they can undergo recombination plays an important role in increasing the genetic variability of the hemiclonal genome and reducing the extinction risk. In this way, hybrid lineages may have survived longer than predicted through occasional recombinant generation.

Why Russia Will Never Make It

The article deals with the complex and multifaceted issue of self-esteem of the Muscovite population. The centuries-old seclusion from Western European processes has forged the psychological type of a ‘lonely people’ constantly looking for its shore but never quite finding it. Such separateness and otherness have led to the cultivation in the public consciousness of a stereotypical higher calling, special mission, mysteriousness, etc. The permanent ‘closed solitude’ has given rise to another psychological phenomenon – suspiciousness and aversion to everything foreign. For the sake of painting an in-depth psychological portrait of Muscovites, the author cites, for instance, controversial thoughts of Nikolai Berdyaev, who analyses the three most important elements of the Russian mindset – its perception of statehood, ethnicity, and religion. Over time, the psychological knots and traumas tied up during the formative stage of the Muscovite nation have eventually transformed into paranoid ideas of its exceptionalism and permissiveness. The author steadily justifies that the psychological type of the Russian people is hazardous for everyone around, particularly for Russia itself. It has not established itself as a democratic, liberal, free, and social state, as it cannot – and will not – do it. Therefore, its internal repressions and international aggression are an evolutionary dead end and a catalyst for collapse. Keywords: Muscovy, psychological type, Berdyaev, Putin, chauvinism, propaganda, rapaciousness.

Sexual Size Dimorphism: Evolution and Perils of Extreme Phenotypes in Spiders.

Sexual size dimorphism is one of the most striking animal traits, and among terrestrial animals, it is most extreme in certain spider lineages. The most extreme sexual size dimorphism (eSSD) is female biased. eSSD itself is probably an epiphenomenon of gendered evolutionary drivers whose strengths and directions are diverse. We demonstrate that eSSD spider clades are aberrant by sampling randomly across all spiders to establish overall averages for female (6.9 mm) and male (5.6 mm) size. At least 16 spider eSSD clades exist. We explore why the literature does not converge on an overall explanation for eSSD and propose an equilibrium model featuring clade- and context-specific drivers of gender size variation. eSSD affects other traits such as sexual cannibalism, genital damage, emasculation, and monogyny with terminal investment. Coevolution with these extreme sexual phenotypes is termed eSSD mating syndrome. Finally, as costs of female gigantism increase with size, eSSD may represent an evolutionary dead end.

Global Patterns of Species Richness in Coastal Cephalopods

Within the context of global climate change and overfishing of fish stocks, there is some evidence that cephalopod populations are benefiting from this changing setting. These invertebrates show enhanced phenotypic flexibility and are found from polar regions to the tropics. Yet, the global patterns of species richness in coastal cephalopods are not known. Here, among the 370 identified-species, 164 are octopuses, 96 are cuttlefishes, 54 are bobtails and bottletails, 48 are inshore squids and 8 are pygmy squids. The most diverse ocean is the Pacific (with 213 cephalopod species), followed by the Indian (146 species) and Atlantic (95 species). The least diverse are the Southern (15 species) and the Arctic (12 species) Oceans. Endemism is higher in the Southern Ocean (87%) and lower in the Arctic (25%), which reflects the younger age and the “Atlantification” of the latter. The former is associated with an old lineage of octopuses that diverged around 33 Ma. Within the 232 ecoregions considered, the highest values of octopus and cuttlefish richness are observed in the Central Kuroshio Current ecoregion (with a total of 64 species), followed by the East China Sea (59 species). This pattern suggests dispersal in the Central Indo-Pacific (CIP) associated with the highly productive Oyashio/Kuroshio current system. In contrast, inshore squid hotspots are found within the CIP, namely in the Sunda Shelf province, which may be linked to the occurrence of an ancient intermittent biogeographic barrier: a land bridge formed during the Pleistocene which severely restricted water flow between the Pacific and Indian Oceans, thereby facilitating squid fauna differentiation. Another marked pattern is a longitudinal richness cline from the Central (CIP) towards the Eastern Indo-Pacific (EIP) realm, with central Pacific archipelagos as evolutionary dead ends. In the Atlantic Ocean, closure of the Atrato Seaway (at the Isthmus of Panama) and Straits of Gibraltar (Mediterranean Sea) are historical processes that may explain the contemporary Caribbean octopus richness and Mediterranean sepiolid endemism, respectively. Last, we discuss how the life cycles and strategies of cephalopods may allow them to adapt quickly to future climate change and extend the borealization of their distribution.

Macroevolution of arboreality in salamanders.

Evolutionary theory predicts that selection in distinct microhabitats generates correlations between morphological and ecological traits, and may increase both phenotypic and taxonomic diversity. However, some microhabitats exert unique selective pressures that act as a restraining force on macroevolutionary patterns of diversification. In this study, we use phylogenetic comparative methods to investigate the evolutionary outcomes of inhabiting the arboreal microhabitat in salamanders. We find that arboreality has independently evolved at least five times in Caudata and has arisen primarily from terrestrial ancestors. However, the rate of transition from arboreality back to terrestriality is 24 times higher than the converse. This suggests that macroevolutionary trends in microhabitat use tend toward terrestriality over arboreality, which influences the extent to which use of the arboreal microhabitat proliferates. Morphologically, we find no evidence for an arboreal phenotype in overall body proportions or in foot shape, as variation in both traits overlaps broadly with species that utilize different microhabitats. However, both body shape and foot shape display reduced rates of phenotypic evolution in arboreal taxa, and evidence of morphological convergence among arboreal lineages is observed. Taken together, these patterns suggest that arboreality has played a unique role in the evolution of this family, providing neither an evolutionary opportunity, nor an evolutionary dead end.

Historical demography of four gecko species specializing in boulder cave habitat: Implications in the evolutionary dead end hypothesis and conservation.

Specialization in narrow ecological niches may not only help species to survive in competitive or unique environments but also contribute to their extermination over evolutionary time. Although the "evolutionary dead end" hypothesis has long been debated, empirical evidence from species with detailed information on niche specialization and evolutionary history remains rare. Here we use a group of four closely related Cnemaspis gecko species that depend highly on granite boulder caves in the Mekong Delta to investigate the potential impact of ecological specialization on their evolution and population dynamics. Isolated by unsuitable floodplain habitats, these boulder-dwelling geckos are among the most narrowly distributed Squamata in the world. We applied several coalescence-based approaches combined with the RAD-seq technique to estimate their divergence times, gene flow and demographic fluctuations during the speciation and population differentiation processes. Our results reveal long-term population shrinkage in the four geckos and limited gene flow during their divergence. The results suggest that the erosion and fragmentation of the granite boulder hills have greatly impacted population divergence and declines. The habitat specialization of these geckos has led to fine-scaled speciation in these granite rocky hills; in contrast, specialization might also have pushed these species toward the edge of extinction. Our study also emphasizes the conservation urgency of these vulnerable, cave-dependent geckos.

Network hubs affect evolvability.

The regulatory processes in cells are typically organized into complex genetic networks. However, it is still unclear how this network structure modulates the evolution of cellular regulation. One would expect that mutations in central and highly connected modules of a network (so-called hubs) would often result in a breakdown and therefore be an evolutionary dead end. However, a new study by Koubkova-Yu and colleagues finds that in some circumstances, altering a hub can offer a quick evolutionary advantage. Specifically, changes in a hub can induce significant phenotypic changes that allow organisms to move away from a local fitness peak, whereas the fitness defects caused by the perturbed hub can be mitigated by mutations in its interaction partners. Together, the results demonstrate how network architecture shapes and facilitates evolutionary adaptation.

One Step up the Ladder of Prebiotic Complexity: Formation of Nonrandom Linear Polypeptides from Binary Systems of Amino Acids on Silica.

Evidence for the formation of linear oligopeptides with nonrandom sequences from mixtures of amino acids coadsorbed on silica and submitted to a simple thermal activation is presented. The amino acid couples (glutamic acid+leucine) and (aspartic acid+valine) were deposited on a fumed silica and submitted to a single heating step at moderate temperature. The evolution of the systems was characterized by X-ray diffraction, infrared spectroscopy, thermosgravimetric analysis, HPLC, and electrospray ionization mass spectrometry (ESI-MS). Evidence for the formation of amide bonds was found in all systems studied. While the products of single amino acids activation on silica could be considered as evolutionary dead ends, (glutamic acid+leucine) and, at to some extent, (aspartic acid+valine) gave rise to the high yield formation of linear peptides up to the hexamers. Oligopeptides of such length have not been observed before in surface polymerization scenarios (unless the amino acids had been deposited by chemical vapor deposition, which is not realistic in a prebiotic environment). Furthermore, not all possible amino acid sequences were present in the activation products, which is indicative of polymerization selectivity. These results are promising for origins of life studies because they suggest the emergence of nonrandom biopolymers in a simple prebiotic scenario.

Fungi between extremotolerance and opportunistic pathogenicity on humans

Numerous agents of infections in humans and other mammals are found among fungi that are able to survive extreme environmental conditions and to quickly adapt to novel habitats. Nevertheless, the relationship between opportunistic potential and polyextremotolerance was not yet studied systematically in fungi. Here, the link between polyextremotolerance and opportunistic pathogenicity is shown in a kingdom-wide phylogenetic analysis as a statistically significant co-occurrence of extremotolerance (e.g. osmotolerance and psychrotolerance) and opportunism at the level of fungal orders. In addition to extremotolerance, fungal opportunists share another characteristic—an apparent lack of specialised virulence traits. This is illustrated by a comparative genomic analysis of 20 dothideomycetous and eurotiomycetous black fungi. While the genomes of specialised fungal plant pathogens were significantly enriched in known virulence-associated genes that encode secreted proteases, carbohydrate active enzyme families, polyketide synthases, and non-ribosomal peptide synthetases, no such signatures were observed in human opportunists. Together the presented results have several implications. If infection of human hosts is a side effect of fungal stress tolerance and adaptability, the human body is most likely neither the preferred habitat of such species, nor important for their evolutionary success. This defines opportunism as opposed to pathogenicity, where infection is advantageous for the species’ fitness. Since opportunists are generally incapable of the host-to-host transmission, any host-specific adaptations are likely to be lost with the resolution of the infection, explaining the observed lack of specialised virulence traits. In this scenario opportunistic infections should be seen as an evolutionary dead end and unlikely to lead to true pathogenicity.

Why are red flowers so rare? Testing the macroevolutionary causes of tippiness.

Traits that have arisen multiple times yet still remain rare present a curious paradox. A number of these rare traits show a distinct tippy pattern, where they appear widely dispersed across a phylogeny, are associated with short branches and differ between recently diverged sister species. This phylogenetic pattern has classically been attributed to the trait being an evolutionary dead end, where the trait arises due to some short-term evolutionary advantage, but it ultimately leads species to extinction. While the higher extinction rate associated with a dead end trait could produce such a tippy pattern, a similar pattern could appear if lineages with the trait speciated slower than other lineages, or if the trait was lost more often that it was gained. In this study, we quantify the degree of tippiness of red flowers in the tomato family, Solanaceae, and investigate the macroevolutionary processes that could explain the sparse phylogenetic distribution of this trait. Using a suite of metrics, we confirm that red-flowered lineages are significantly overdispersed across the tree and form smaller clades than expected under a null model. Next, we fit 22 alternative models using HiSSE (Hidden State Speciation and Extinction), which accommodates asymmetries in speciation, extinction and transition rates that depend on observed and unobserved (hidden) character states. Results of the model fitting indicated significant variation in diversification rates across the family, which is best explained by the inclusion of hidden states. Our best fitting model differs between the maximum clade credibility tree and when incorporating phylogenetic uncertainty, suggesting that the extreme tippiness and rarity of red Solanaceae flowers makes it difficult to distinguish among different underlying processes. However, both of the best models strongly support a bias towards the loss of red flowers. The best fitting HiSSE model when incorporating phylogenetic uncertainty lends some support to the hypothesis that lineages with red flowers exhibit reduced diversification rates due to elevated extinction rates. Future studies employing simulations or targeting population-level processes may allow us to determine whether red flowers in Solanaceae or other angiosperms clades are rare and tippy due to a combination of processes, or asymmetrical transitions alone.

Estimating divergence times and ancestral breeding systems in Ficus and Moraceae.

Although dioecy, which characterizes only 6 % of angiosperm species, has been considered an evolutionary dead end, recent studies have demonstrated that this is not necessarily the case. Moraceae (40 genera, 1100 spp., including Ficus, 750 spp.) are particularly diverse in breeding systems (including monoecy, gynodioecy, androdioecy and dioecy) and thus represent a model clade to study macroevolution of dioecy. Ancestral breeding systems of Ficus and Moraceae were inferred. To do so, a new dated phylogenetic tree of Ficus and Moraceae was first reconstructed by combining a revised 12-fossil calibration set and a densely sampled molecular data set of eight markers and 320 species. Breeding system evolution was then reconstructed using both parsimony and model-based (maximum likelihood and Bayesian) approaches with this new time scale. The crown group ages of Ficus and Moraceae were estimated in the Eocene (40.6-55.9 Ma) and Late Cretaceous (73.2-84.7 Ma), respectively. Strong support was found for ancestral dioecy in Moraceae. Although the ancestral state of Ficus remained particularly sensitive to model selection, the results show that monoecy and gynodioecy evolved from dioecy in Moraceae, and suggest that gynodioecy probably evolved from monoecy in Ficus. Dioecy was found not to be an evolutionary dead end in Moraceae. This study provides a new time scale for the phylogeny and a new framework of breeding system evolution in Ficus and Moraceae.