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BMC Evol Biol [journal]
- Cretaceous environmental changes led to high extinction rates in a hyperdiverse beetle family. [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Oct 21; 14(1):220.
BackgroundAs attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms. A major biome turnover that occurred during this period was the rise of angiosperms starting ca. 125 million years ago. Though there is evidence that the latter promoted the diversification of phytophagous insects, the response of other insect groups to Cretaceous environmental changes is still largely unknown. To gain novel insights on this issue, we assess the diversification dynamics of a hyperdiverse family of detritivorous beetles (Tenebrionidae) using molecular dating and diversification analyses.ResultsAge estimates reveal an origin after the Triassic-Jurassic mass extinction (older than previously thought), followed by the diversification of major lineages during Pangaean and Gondwanan breakups. Dating analyses indicate that arid-adapted species diversified early, while most of the lineages that are adapted to more humid conditions diversified much later. Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates.ConclusionsWe hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.
- Ingestion of radioactively contaminated diets for two generations in the pale grass blue butterfly. [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Sep 23; 14(1):193.
The release of radioactive materials due to the Fukushima nuclear accident has raised concern regarding the biological impacts of ingesting radioactively contaminated diets on organisms. We previously performed an internal exposure experiment in which contaminated leaves collected from polluted areas were fed to larvae of the pale grass blue butterfly, Zizeeria maha, from Okinawa, which is one of the least polluted localities in Japan. Using the same experimental system, in the present study, we further examined the effects of low-level-contaminated diets on this butterfly. Leaves were collected from two localities in Tohoku (Motomiya (161 Bq/kg) and Koriyama (117 Bq/kg)); two in Kanto (Kashiwa (47.6 Bq/kg) and Musashino (6.4 Bq/kg)); one in Tokai (Atami (2.5 Bq/kg)); and from Okinawa (0.2 Bq/kg). In addition to the effects on the first generation, we examined the possible transgenerational effects of the diets on the next generation.In the first generation, the Tohoku groups showed higher rates of mortality and abnormalities and a smaller forewing size than the Okinawa group. The mortality rates were largely dependent on the ingested dose of caesium. The survival rates of the Kanto-Tokai groups were greater than 80%, but the rates in the Tohoku groups were much lower. In the next generation, the survival rates in the Tohoku groups were below 20%, whereas those of the Okinawa groups were above 70%. The survival rates in the second generation were independent of the locality of the leaves ingested by the first generation, indicating that the diet in the second generation was the determinant of their survival. Moreover, a smaller forewing size was observed in the Tohoku groups in the second generation. However, the forewing size was inversely correlated with the cumulative caesium dose ingested throughout the first and second generations, indicating that the diet in the first generation also influenced the forewing size of the second generation.Biological effects are detectable under a low ingested dose of radioactivity from a contaminated diet. The effects are transgenerational but can be overcome by ingesting a non-contaminated diet, suggesting that at least some of the observed effects are attributable to non-genetic physiological changes.
- Neofunctionalization of a duplicate hatching enzyme gene during the evolution of teleost fishes. [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Oct 19; 14(1):221.
BackgroundDuplication and subsequent neofunctionalization of the teleostean hatching enzyme gene occurred in the common ancestor of Euteleostei and Otocephala, producing two genes belonging to different phylogenetic clades (clades I and II). In euteleosts, the clade I enzyme inherited the activity of the ancestral enzyme of swelling the egg envelope by cleavage of the N-terminal region of egg envelope proteins. The clade II enzyme gained two specific cleavage sites, N-ZPd and mid-ZPd but lost the ancestral activity. Thus, euteleostean clade II enzymes assumed a new function; solubilization of the egg envelope by the cooperative action with clade I enzyme. However, in Otocephala, the clade II gene was lost during evolution. Consequently, in a late group of Otocephala, only the clade I enzyme is present to swell the egg envelope. We evaluated the egg envelope digestion properties of clade I and II enzymes in Gonorynchiformes, an early diverging group of Otocephala, using milkfish, and compared their digestion with those of other fishes. Finally, we propose a hypothesis the neofunctionalization process.ResultsThe milkfish clade II enzyme cleaved N-ZPd but not mid-ZPd, and did not cause solubilization of the egg envelope. We conclude that neofunctionalization is incomplete in the otocephalan clade II enzymes. Comparison of clade I and clade II enzyme characteristics implies that the specificity of the clade II enzymes gradually changed during evolution after the duplication event, and that a change in substrate was required for the addition of the mid-ZPd site and loss of activity at the N-terminal region.ConclusionsWe infer the process of neofunctionalization of the clade II enzyme after duplication of the gene. The ancestral clade II gene gained N-ZPd cleavage activity in the common ancestral lineage of the Euteleostei and Otocephala. Subsequently, acquisition of cleavage activity at the mid-ZPd site and loss of cleavage activity in the N-terminal region occurred during the evolution of Euteleostei, but not of Otocephala. The clade II enzyme provides an example of the development of a neofunctional gene for which the substrate, the egg envelope protein, has adapted to a gradual change in the specificity of the corresponding enzyme.
- Complex body size trends in the evolution of sloths (Xenarthra: Pilosa). [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Sep 10; 14(1):184.
Extant sloths present an evolutionary conundrum in that the two living genera are superficially similar (small-bodied, folivorous, arboreal) but diverged from one another approximately 30 million years ago and are phylogenetically separated by a radiation of medium to massive, mainly ground-dwelling, taxa. Indeed, the species in the two living genera are among the smallest, and perhaps most unusual, of the 50+ known sloth species, and must have independently and convergently evolved small size and arboreality. In order to accurately reconstruct sloth evolution, it is critical to incorporate their extinct diversity in analyses. Here, we used a dataset of 57 species of living and fossil sloths to examine changes in body mass mean and variance through their evolution, employing a general time-variable model that allows for analysis of evolutionary trends in continuous characters within clades lacking fully-resolved phylogenies, such as sloths.Our analyses supported eight models, all of which partition sloths into multiple subgroups, suggesting distinct modes of body size evolution among the major sloth lineages. Model-averaged parameter values supported trended walks in most clades, with estimated rates of body mass change ranging as high as 126 kg/million years for the giant ground sloth clades Megatheriidae and Nothrotheriidae. Inclusion of living sloth species in the analyses weakened reconstructed rates for their respective groups, with estimated rates for Megalonychidae (large to giant ground sloths and the extant two-toed sloth) were four times higher when the extant genus Choloepus was excluded.Analyses based on extant taxa alone have the potential to oversimplify or misidentify macroevolutionary patterns. This study demonstrates the impact that integration of data from the fossil record can have on reconstructions of character evolution and establishes that body size evolution in sloths was complex, but dominated by trended walks towards the enormous sizes exhibited in some recently extinct forms.
- Morphological differentiation despite gene flow in an endangered grasshopper. [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Oct 16; 14(1):216.
BackgroundGene flow is traditionally considered a limitation to speciation because selection is required to counter the homogenising effect of allele exchange. Here we report on two sympatric short-horned grasshoppers species in the South Island of New Zealand; one (Sigaus australis) widespread and the other (Sigaus childi) a narrow endemic.ResultsOf the 79 putatively neutral markers (mtDNA, microsatellite loci, ITS sequences and RAD-seq SNPs) all but one marker we examined showed extensive allele sharing, and similar or identical allele frequencies in the two species where they co-occur. We found no genetic evidence of deviation from random mating in the region of sympatry. However, analysis of morphological and geometric traits revealed no evidence of morphological introgression.ConclusionsBased on phenotype the two species are clearly distinct, but their genotypes thus far reveal no divergence. The best explanation for this is that some loci associated with the distinguishing morphological characters are under strong selection, but exchange of neutral loci is occurring freely between the two species. Although it is easier to define species as requiring a barrier between them, a dynamic model that accommodates gene flow is a biologically more reasonable explanation for these grasshoppers.
- The strange case of East African annual fish: aridification correlates with diversification for a savannah aquatic group? [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Oct 14; 14(1):210.
BackgroundAnnual Nothobranchius fish are distributed in East and Southern Africa and inhabit ephemeral pools filled during the monsoon season. Nothobranchius show extreme life-history adaptations: embryos survive by entering diapause and they are the vertebrates with the fastest maturation and the shortest lifespan. The distribution area of Nothobranchius overlaps with the East Africa Rift System. The geological and paleoclimatic history of this region is known in detail: in particular, aridification of East Africa and expansion of grassland habitats started 8 Mya and three humid periods between 3 and 1 Mya are superimposed on the longer-term aridification. These climatic oscillations are thought to have shaped evolution of savannah African mammals. We reconstructed the phylogeny of Nothobranchius and dated the different stages of diversification in relation to these paleoclimatic events.ResultsWe sequenced one mitochondrial locus and five nuclear loci in 63 specimens and obtained a robust phylogeny. Nothobranchius can be divided in four geographically separated clades whose boundaries largely correspond to the East Africa Rift system. Statistical analysis of dispersal and vicariance identifies a Nilo-Sudan origin with southwards dispersion and confirmed that these four clades are the result of vicariance events In the absence of fossil Nothobranchius, molecular clock was calibrated using more distant outgroups (secondary calibration). This method estimates the age of the Nothobranchius genus to be 8.3 (6.0 ¿ 10.7) My and the separation of the four clades 4.8 (2.7-7.0) Mya. Diversification within the clades was estimated to have started ~3 Mya and most species pair were estimated to have an age of 0.5-1 My.ConclusionsThe mechanism of Nothobranchius diversification was allopatric and driven by geographic isolation. We propose a scenario where diversification of Nothobranchius started in rough coincidence with aridification of East Africa, establishment of grassland habitats and the appearance of the typical African bovid fauna of the savannah. Although confidence intervals for the estimated ages of the four Nothobranchius clades are quite large, this scenario is compatible with the biology of extant Nothobrachius that are critically dependent on savannah habitats. Therefore, Nothobranchius diversification might have been shaped by the same paleoclimatic events that shaped African ungulate evolution.
- The loss of taste genes in cetaceans. [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Oct 12; 14(1):218.
BackgroundFive basic taste modalities, sour, sweet, bitter, salt and umami, can be distinguished by humans and are fundamental for physical and ecological adaptations in mammals. Molecular genetic studies of the receptor genes for these tastes have been conducted in terrestrial mammals; however, little is known about the evolution and adaptation of these genes in marine mammals.ResultsHere, all five basic taste modalities, sour, sweet, bitter, salt and umami, were investigated in cetaceans. The sequence characteristics and evolutionary analyses of taste receptor genes suggested that nearly all cetaceans may have lost all taste modalities except for that of salt.ConclusionsThis is the first study to comprehensively examine the five basic taste modalities in cetaceans with extensive taxa sampling. Our results suggest that cetaceans have lost four of the basic taste modalities including sour, sweet, umami, and most of the ability to sense bitter tastes. The integrity of the candidate salt taste receptor genes in all the cetaceans examined may be because of their function in Na+ reabsorption, which is key to osmoregulation and aquatic adaptation.
- Western Eurasian ancestry in modern Siberians based on mitogenomic data. [Journal Article]
- BMC Evol Biol 2014.:217.
Although the genetic heritage of aboriginal Siberians is mostly of eastern Asian ancestry, a substantial western Eurasian component is observed in the majority of northern Asian populations. Traces of at least two migrations into southern Siberia, one from eastern Europe and the other from western Asia/the Caucasus have been detected previously in mitochondrial gene pools of modern Siberians.We report here 166 new complete mitochondrial DNA (mtDNA) sequences that allow us to expand and re-analyze the available data sets of western Eurasian lineages found in northern Asian populations, define the phylogenetic status of Siberian-specific subclades and search for links between mtDNA haplotypes/subclades and events of human migrations. From a survey of 158 western Eurasian mtDNA genomes found in Siberia we estimate that nearly 40% of them most likely have western Asian and another 29% European ancestry. It is striking that 65 of northern Asian mitogenomes, i.e. ~41%, fall into 19 branches and subclades which can be considered as Siberian-specific being found so far only in Siberian populations. From the coalescence analysis it is evident that the sequence divergence of Siberian-specific subclades was relatively small, corresponding to only 0.6-9.5 kya (using the complete mtDNA rate) and 1-6 kya (coding region rate).The phylogeographic analysis implies that the western Eurasian founders, giving rise to Siberian specific subclades, may trace their ancestry only to the early and mid-Holocene, though some of genetic lineages may trace their ancestry back to the end of Last Glacial Maximum (LGM). We have not found the modern northern Asians to have western Eurasian genetic components of sufficient antiquity to indicate traces of pre-LGM expansions.
- Recovering species demographic history from multi-model inference: the case of a Neotropical savanna tree species. [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Oct 11; 14(1):213.
BackgroundGlaciations were recurrent throughout the Quaternary and potentially shaped species genetic structure worldwide by affecting population dynamics. Here, we implemented a multi-model inference approach to recover the distribution dynamics and demographic history of a Neotropical savanna tree, Tabebuia aurea (Bignoniaceae). Exploring different algorithms and paleoclimatic simulations, we used ecological niche modelling to generate alternative hypotheses of potential demographic changes through the last glacial cycle and estimated genetic parameters using coalescent modelling.ResultsComparing predictions from demographic hypotheses with genetic parameters of modern populations, our findings revealed a likely scenario of population decline, with spatial displacement towards Northeast Brazil from the last glacial maximum to the mid-Holocene. Subsequently, populations expanded in response to the return of the climatically suitable conditions in Central-West Brazil. Nevertheless, a wide historical refugium across Central Brazil likely maintained large populations connected throughout time. The expected genetic signatures from such predicted distribution dynamics are also corroborated by spatial genetic structure observed in modern populations.ConclusionBy exploring uncertainties inherent in multiple working hypotheses, we have shown that multi-model inference is a fruitful and efficient approach to recover the nature, timing and geographical context of the Tabebuia aurea population dynamic in response to the Quaternary climate changes.
- Ecological niche and phylogeography elucidate complex biogeographic patterns in Loxosceles rufescens (Araneae, Sicariidae) in the Mediterranean Basin. [JOURNAL ARTICLE]
- BMC Evol Biol 2014 Oct 9; 14(1):195.
BackgroundUnderstanding the evolutionary history of morphologically cryptic species complexes is difficult, and made even more challenging when geographic distributions have been modified by human-mediated dispersal. This situation is common in the Mediterranean Basin where, aside from the environmental heterogeneity of the region, protracted human presence has obscured the biogeographic processes that shaped current diversity. Loxosceles rufescens (Araneae, Sicariidae) is an ideal example: native to the Mediterranean, the species has dispersed worldwide via cohabitation with humans. A previous study revealed considerable molecular diversity, suggesting cryptic species, but relationships among lineages did not correspond to geographic location.ResultsDelimitation analyses on cytochrome c oxidase subunit I identified 11 different evolutionary lineages, presenting two contrasting phylogeographic patterns: (1) lineages with well-structured populations in Morocco and Iberia, and (2) lineages lacking geographic structure across the Mediterranean Basin. Dating analyses placed main diversification events in the Pleistocene, and multiple Pleistocene refugia, identified using ecological niche modeling (ENM), are compatible with allopatric differentiation of lineages. Human-mediated transportation appears to have complicated the current biogeography of this medically important and synanthropic spider.ConclusionsWe integrated ecological niche models with phylogeographic analyses to elucidate the evolutionary history of L. rufescens in the Mediterranean Basin, with emphasis on the origins of mtDNA diversity. We found support for the hypothesis that northern Africa was the center of origin for L. rufescens, and that current genetic diversity originated in allopatry, likely promoted by successive glaciations during the Pleistocene. We corroborated the scenario of multiple refugia within the Mediterranean, principally in northern Africa, combining results from eight atmosphere¿ocean general circulation models (AOGCMs) with two different refugium-delimitation methodologies. ENM results were useful for providing general views of putative refugia, with fine-scale details depending on the level of stringency applied for agreement among models.