Increased rate of hair keratin gene loss in the cetacean lineage

Background

Hair represents an evolutionary innovation that appeared early on mammalian evolutionary history, and presumably contributed significantly to the rapid radiation of the group. An interesting event in hair evolution has been its secondary loss in some mammalian groups, such as cetaceans, whose hairless phenotype appears to be an adaptive response to better meet the environmental conditions. To determine whether different repertoire of keratin genes among mammals can potentially explain the phenotypic hair features of different lineages, we characterized the type I and II clusters of alpha keratins from eight mammalian species, including the hairless dolphin and minke whale representing the order Cetacea.

Results

We combined the available genomic information with phylogenetic analysis to conduct a comprehensive analysis of the evolutionary patterns of keratin gene clusters. We found that both type I and II gene clusters are fairly conserved among the terrestrial mammals included in this study, with lineage specific gene duplication and gene loss. Nevertheless, there is also evidence for an increased rate of pseudogenization in the cetacean lineage when compared to their terrestrial relatives, especially among the hair type keratins.

Conclusions

Here we present a comprehensive characterization of alpha-keratin genes among mammals and elucidate the mechanisms involved in the evolution of this gene family. We identified lineage-specific gene duplications and gene loss among the Laurasiatherian and Euarchontoglires species included in the study. Interestingly, cetaceans present an increased loss of hair-type keratin genes when compared to other terrestrial mammals. As suggested by the ‘less-is-more’ hypothesis, we do not rule out the possibility that the gene loss of hair-type keratin genes in these species might be associated to the hairless phenotype and could have been adaptive in response to new selective pressures imposed by the colonization of a new habitat. Our study provides support for the idea that pseudogenes are not simply ‘genomic fossils’ but instead have adaptive roles during the evolutionary process.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-869) contains supplementary material, which is available to authorized users.     

Mammalian keratin associated proteins (KRTAPs) subgenomes: disentangling hair diversity and adaptation to terrestrial and aquatic environments

Background

Adaptation of mammals to terrestrial life was facilitated by the unique vertebrate trait of body hair, which occurs in a range of morphological patterns. Keratin associated proteins (KRTAPs), the major structural hair shaft proteins, are largely responsible for hair variation.

Results

We exhaustively characterized the KRTAP gene family in 22 mammalian genomes, confirming the existence of 30 KRTAP subfamilies evolving at different rates with varying degrees of diversification and homogenization. Within the two major classes of KRTAPs, the high cysteine (HS) subfamily experienced strong concerted evolution, high rates of gene conversion/recombination and high GC content. In contrast, high glycine-tyrosine (HGT) KRTAPs showed evidence of positive selection and low rates of gene conversion/recombination. Species with more hair and of higher complexity tended to have more KRATP genes (gene expansion). The sloth, with long and coarse hair, had the most KRTAP genes (175 with 141 being intact). By contrast, the “hairless” dolphin had 35 KRTAPs and the highest pseudogenization rate (74% relative to the 19% mammalian average). Unique hair-related phenotypes, such as scales (armadillo) and spines (hedgehog), were correlated with changes in KRTAPs. Gene expression variation probably also influences hair diversification patterns, for example human have an identical KRTAP repertoire as apes, but much less hair.

Conclusions

We hypothesize that differences in KRTAP gene repertoire and gene expression, together with distinct rates of gene conversion/recombination, pseudogenization and positive selection, are likely responsible for micro and macro-phenotypic hair diversification among mammals in response to adaptations to ecological pressures.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-779) contains supplementary material, which is available to authorized users.     

Avian sebokeratocytes and marine mammal lipokeratinocytes: structural, lipid biochemical, and functional considerations

In terrestrial mammals, stratum corneum lipids derive from two sources: deposition of lamellar body lipids in stratum corneum interstices and excretion of sebaceous lipids onto the skin surface, resulting in a two-compartment ("bricks and mortar") system of lipid-depleted cells surrounded by lipid-enriched intercellular spaces. In contrast, intracellular lipid droplets, normally not present in the epidermis of terrestrial mammals, are prominent in avian and marine mammal epidermis (cetaceans, manatees). We compared the transepidermal water loss, ultrastructure, and lipid biochemistry of the viable epidermis and stratum corneum of pigeon apterium, fledgling (featherless) zebra finches, painted storks, cetaceans, and manatees to those of humans and mice. Marine mammals possess an even more extensive lamellar-body secretory system than do terrestrial mammals; and lamellar-body contents, as in terrestrials, are secreted into the stratum corneum interstices. In cetaceans, however, glycolipids, but not ceramides, persist into the stratum corneum; whereas in manatees, glycolipids are replaced by ceramides, as in terrestrial mammals. Acylglucosylceramides, thought to be critical for lamellar-body deposition and barrier function in terrestrial mammals, are present in manatees but virtually absent in cetaceans, a finding that indicates that they are not obligate constituents of lamellar-body-derived membrane structures. Moreover, cetaceans do not elaborate the very long-chain, saturated N-acyl fatty acids that abound in terrestrial mammalian acylglucosylceramides. Furthermore, cold-water marine mammals generate large, intracellular neutral lipid droplets not found in terrestrial and warm-water marine mammals; these lipid droplets persist into the stratum corneum, suggesting thermogenesis, flotation, and/or cryoprotectant functions. Avians generate distinctive multigranular bodies that may be secreted into the intercellular spaces under xerotic conditions, as in zebra fledglings; ordinarily, however, the internal lamellae and limiting membranes deteriorate, generating intracellular neutral lipid droplets. The sphingolipid composition of avian stratum corneum is intermediate between terrestrials and cetaceans (approximately equal to 50% glycolipids), with triglycerides present in abundance. In the midstratum corneum of avians, neutral lipid droplets are released into the interstices, forming a large extracellular, lipid-enriched compartment, surrounding wafer-thin corneocytes, with a paucity of both lipid and keratin ("plates-and-mortar" rather than the "bricks-and-mortar" of mammals).(ABSTRACT TRUNCATED AT 400 WORDS)     

The vestigial olfactory receptor subgenome of odontocete whales: phylogenetic congruence between gene-tree reconciliation and supermatrix methods

The macroevolutionary transition of whales (cetaceans) from a terrestrial quadruped to an obligate aquatic form involved major changes in sensory abilities. Compared to terrestrial mammals, the olfactory system of baleen whales is dramatically reduced, and in toothed whales is completely absent. We sampled the olfactory receptor (OR) subgenomes of eight cetacean species from four families. A multigene tree of 115 newly characterized OR sequences from these eight species and published data for Bos taurus revealed a diverse array of class II OR paralogues in Cetacea. Evolution of the OR gene superfamily in toothed whales (Odontoceti) featured a multitude of independent pseudogenization events, supporting anatomical evidence that odontocetes have lost their olfactory sense. We explored the phylogenetic utility of OR pseudogenes in Cetacea, concentrating on delphinids (oceanic dolphins), the product of a rapid evolutionary radiation that has been difficult to resolve in previous studies of mitochondrial DNA sequences. Phylogenetic analyses of OR pseudogenes using both gene-tree reconciliation and supermatrix methods yielded fully resolved, consistently supported relationships among members of four delphinid subfamilies. Alternative minimizations of gene duplications, gene duplications plus gene losses, deep coalescence events, and nucleotide substitutions plus indels returned highly congruent phylogenetic hypotheses. Novel DNA sequence data for six single-copy nuclear loci and three mitochondrial genes (> 5000 aligned nucleotides) provided an independent test of the OR trees. Nucleotide substitutions and indels in OR pseudogenes showed a very low degree of homoplasy in comparison to mitochondrial DNA and, on average, provided more variation than single-copy nuclear DNA. Our results suggest that phylogenetic analysis of the large OR superfamily will be effective for resolving relationships within Cetacea whether supermatrix or gene-tree reconciliation procedures are used.     

Decay of TRPV3 as the genomic trace of epidermal structure changes in the land‐to‐sea transition of mammals

The epidermis plays an indispensable barrier function in animals. Some species have evolved unique epidermal structures to adapt to different environments. Aquatic and semi‐aquatic mammals (cetaceans, manatees, and hippopotamus) are good models to study the evolution of epidermal structures because of their exceptionally thickened stratum spinosum, the lack of stratum granulosum, and the parakeratotic stratum corneum. This study aimed to analyze an upstream regulatory gene transient receptor potential cation channel, subfamily V, member 3 (TRPV3) of epidermal differentiation so as to explore the association between TRPV3 evolution and epidermal changes in mammals. Inactivating mutations were detected in almost all the aquatic cetaceans and several terrestrial mammals. Relaxed selective pressure was examined in the cetacean lineages with inactivated TRPV3, which might contribute to its exceptionally thickened stratum spinosum as the significant thickening of stratum spinosum in TRPV3 knock‐out mouse. However, functional TRPV3 may exist in several terrestrial mammals due to their strong purifying selection, although they have “inactivating mutations.” Further, for intact sequences, relaxed selective constraints on the TRPV3 gene were also detected in aquatic cetaceans, manatees, and semi‐aquatic hippopotamus. However, they had intact TRPV3, suggesting that the accumulation of inactivating mutations might have lagged behind the relaxed selective pressure. The results of this study revealed the decay of TRPV3 being the genomic trace of epidermal development in aquatic and semi‐aquatic mammals. They provided insights into convergently evolutionary changes of epidermal structures during the transition from the terrestrial to the aquatic environment.     

Manatees as Sentinels of Marine Ecosystem Health: Are They the 2000-pound Canaries?

The order Sirenia is represented by three species of manatees and one species of dugong distributed in tropical and subtropical regions of the world and considered vulnerable to extinction. The sentinel species concept is useful to identify indicators of the environment and may reflect the quality of health in marine ecosystems. The single species approach to evaluate ecological health may provide a series of snap shots of environmental changes to determine if animal, human, or ecosystem health may be affected. Under this concept, marine vertebrates may be good integrators of changes over space and time, and excellent sentinels of ecosystem health. Based on their life history, manatees may or may not be ideal sentinels, as they are robust, long-lived species and appear remarkably resilient to natural disease and the effects of human-related injury and trauma. These characteristics might be the result of an efficient and responsive immune system compared to other marine mammals. Although relatively immune to infectious agents, manatees face other potentially serious threats, including epizootic diseases and pollution while in large aggregations. Manatees can serve as excellent sentinels of harmful algal blooms due to their high sensitivity, specifically to brevetoxicosis, which has caused at least two major die-offs in recent times. Threats to manatees worldwide, such as illegal hunting and boat collisions, are increasing. Habitat is being lost at an alarming rate and the full effects of uncontrolled human population growth on the species are unknown. The manatee may serve as a sentinel species, prognosticating the deleterious effects of unhealthy marine and aquatic ecosystems on humans. We have identified a number of critical research needs and opportunities for transdisciplinary collaboration that could help advance the use of the sentinel species concept in marine ecosystem health and monitoring of disease emergence using our knowledge on these magnificent sirenians.     

Impact of the terrestrial-aquatic transition on disparity and rates of evolution in the carnivoran skull

Background

Which factors influence the distribution patterns of morphological diversity among clades? The adaptive radiation model predicts that a clade entering new ecological niche will experience high rates of evolution early in its history, followed by a gradual slowing. Here we measure disparity and rates of evolution in Carnivora, specifically focusing on the terrestrial-aquatic transition in Pinnipedia. We analyze fissiped (mostly terrestrial, arboreal, and semi-arboreal, but also including the semi-aquatic otter) and pinniped (secondarily aquatic) carnivorans as a case study of an extreme ecological transition. We used 3D geometric morphometrics to quantify cranial shape in 151 carnivoran specimens (64 fissiped, 87 pinniped) and five exceptionally-preserved fossil pinnipeds, including the stem-pinniped Enaliarctos emlongi. Range-based and variance-based disparity measures were compared between pinnipeds and fissipeds. To distinguish between evolutionary modes, a Brownian motion model was compared to selective regime shifts associated with the terrestrial-aquatic transition and at the base of Pinnipedia. Further, evolutionary patterns were estimated on individual branches using both Ornstein-Uhlenbeck and Independent Evolution models, to examine the origin of pinniped diversity.

Results

Pinnipeds exhibit greater cranial disparity than fissipeds, even though they are less taxonomically diverse and, as a clade nested within fissipeds, phylogenetically younger. Despite this, there is no increase in the rate of morphological evolution at the base of Pinnipedia, as would be predicted by an adaptive radiation model, and a Brownian motion model of evolution is supported. Instead basal pinnipeds populated new areas of morphospace via low to moderate rates of evolution in new directions, followed by later bursts within the crown-group, potentially associated with ecological diversification within the marine realm.

Conclusion

The transition to an aquatic habitat in carnivorans resulted in a shift in cranial morphology without an increase in rate in the stem lineage, contra to the adaptive radiation model. Instead these data suggest a release from evolutionary constraint model, followed by aquatic diversifications within crown families.

Electronic supplementary material

The online version of this article (doi:10.1186/s12862-015-0285-5) contains supplementary material, which is available to authorized users.     

TLR4 and TLR8 variability in Amazonian and West Indian manatee species from Brazil

Amazonian (Trichechus inunguis) and West Indian (Trichechus manatus) manatees are aquatic mammals vulnerable to extinction found in the Amazon basin and the coastal western Atlantic. Toll-like receptors (TLR) play a key role in recognizing pathogen-associated molecular patterns using leucine-rich repeats (LRRs). We described the diversity of TLR4 and TLR8 genes in these two species of manatee. Amazonian manatee showed seven SNPs in TLR4 and the eight in TLR8, while West Indian manatee shared four and six of those SNPs, respectively. In our analysis, TLR4 showed one non-conservative amino acid replacement substitution in LRR7 and LRR8, on the other hand, TLR8 was less variable and showed only conserved amino acid substitutions. Selection analysis showed that only one TLR4 site was subjected to positive selection and none in TLR8. TLR4 in manatees did not show any evidence of convergent evolution compared to species of the cetacean lineage. Differences in TLR4 and TLR8 polymorphism may be related to distinct selection by pathogens, population reduction of West Indian manatees, or an expected consequence of population expansion in Amazonian manatees. Future studies combining pathogen association and TLR polymorphism may clarify possible roles of these genes and be used for conservation purposes of manatee species.     

The existence value of the Antillean manatee in the unprotected Hondo River (Mexico) as a fundamental component for its conservation

The Hondo River is the natural border between Mexico and Belize, and it is part of the distribution area of the Endangered Antillean manatee Trichechus manatus manatus. Currently, the Hondo River does not have any special protection. Employing qualitative research methods, we documented the social perception and local knowledge from riverside communities to assess conservation status and trends of manatees in the area. Fifty semi-structured interviews were carried out to river users in 16 Mexican communities, distributed in six segments along the riverbed. The claims of the inhabitants agree with boat-based surveys: most of the current and historical manatee sightings were reported in segments of the main watercourses, but also in small tributaries, which are usually shallow and rich in aquatic vegetation. Additionally, the local perception about manatee conservation status can be helpful to understand population trends and threats: 48 % of the interviewees claimed that nowadays the number of sighted manatees is less than that observed 10 years ago. The responders identified water pollution due to cane cultivation practices, motorized vessels traffic, and presence of fishing nets as potential threats to manatees. This study provides evidence of relevant local knowledge about the manatee ecology and its habitat, critical in the construction of binational conservation strategies for the species. Therefore, local resources users may play an increasingly significant role in manatee management and monitoring. Although manatees are poached for their meat in several areas of their distribution, the most common value attributed to manatees in Hondo River was non-use existence values. Local people recognize the challenges to observe this cryptic species in this river, but also identified manatees as potential flag species, suggesting that it may represent a valuable resource for ecotourism. We suggest that the non-extractive use of manatees has the potential for promoting species conservation and local economic growth.     

PREHENSILE USE OF PERIORAL BRISTLES DURING FEEDING AND ASSOCIATED BEHAVIORS OF THE FLORIDA MANATEE (TRICHECHUS MANATUS LATIROSTRIS)

The use of perioral bristles (modified vibrissae) by 17 captive Florida manatees and approximately 20 wild manatees was analyzed. Captive manatees were fed six species of aquatic vegetation normally eaten in the wild (four freshwater species and two seagrasses). Inanimate objects were placed in the holding tanks with manatees at Lowry Park Zoological Gardens (Tampa, FL) to determine the degree to which perioral bristles were used in exploration and to define the range of manipulative behavior. In addition, behavioral observations were made on the use of perioral bristles during social interactions with conspecifics. Observations were recorded using a Hi8-format video camera. Florida manatees possess an unusually large degree of fine motor control of the snout and perioral bristles. The large and robust perioral bristle fields of the upper lip were used in a prehensile manner during feeding. Bristle use by manatees feeding on submerged vegetation differed from that seen during feeding on floating vegetation. Other behavioral use of the perioral bristles shows variation depending upon the situation encountered. The degree of plasticity of perioral bristle use supports our hypothesis that the vibrissal-muscular complex of the Florida manatee has evolved to increase the efficiency of grazing and browsing on aquatic vegetation and to fully maximize the potential of the manatee as a generalist feeder. The manipulative and sensitive nature of the manatee snout is likely a manifestation of a complex sensory and motor system which has evolved for marine mammal aquatic herbivores living in shallow turbid habitats.     

Life cycle impacts of topsoil erosion on aquatic biota: case study on <Emphasis Type="Italic">Eucalyptus globulus</Emphasis> forest

Purpose

This study illustrates the applicability of a framework to conduct a spatially distributed inventory of suspended solids (SS) delivery to freshwater streams combined with a method to derive site-specific characterisation factors for endpoint damage on aquatic ecosystem diversity. A case study on Eucalyptus globulus stands located in Portugal was selected as an example of a land-based system. The main goal was to assess the relevance of SS delivery to freshwater streams, providing a more comprehensive assessment of the SS impact from land use systems on aquatic environments.

Methods

The WaTEM/SEDEM model, which was used to perform the SS inventory, is a raster-based empirical erosion and deposition model. This model allowed to predict the amount of SS from E. globulus stands under study and route this amount through the landscape towards the drainage network. Combining the spatially explicit SS inventory with the derived site-specific endpoint characterisation factors of SS delivered to two different river sections, the potential damages of SS on macroinvertebrates, algae and macrophytes were assessed. In addition, this damage was compared with the damage obtained with the commonly used ecosystem impact categories of the ReCiPe method.

Results and discussion

The relevance of the impact from SS delivery to freshwater streams is shown, providing a more comprehensive assessment of the SS impact from land use systems on aquatic environments. The SS impacts ranged from 15.5 to 1234.9 PDF m³.yr.ha^?1.revolution^?1 for macroinvertebrates, and from 5.2 to 411.9 PDF.m³.yr.ha^?1.revolution^?1 for algae and macrophytes.For some stands, SS potential impacts on macroinvertebrates have the same order of magnitude than freshwater eutrophication, freshwater ecotoxicity, terrestrial ecotoxicity and terrestrial acidification impacts. For algae and macrophytes, most of the stands present SS impacts of the same order of magnitude as terrestrial ecotoxicity, one order of magnitude higher than freshwater eutrophication and two orders of magnitude lower than freshwater ecotoxicity and terrestrial acidification.

Conclusions

The SS impact results allow concluding that the increase of SS in the water column can cause biodiversity damage and that the calculated impacts can have a similar or even higher contribution to the total environmental impact than the commonly used ecosystem impact categories of the ReCiPe method. A wide application of the framework and method developed at a local scale will enable the establishment of a regionalised SS inventory database and a deep characterisation of the potential environmental impacts of SS on local aquatic environments.

     

A review of Killer Whale interactions with other marine mammals: predation to co-existence

Killer Whales are well-known as predators of other marine mammals, including the large Sperm and baleen whales. Members of all marine mammal families, except the river dolphins and manatees, have been recorded as prey of Killer Whales; attacks have been observed on 20 species of cetaceans, 14 species of pinnipeds, the Sea Otter, and the Dugong. Ecological interactions have not been systematically studied and further work may indicate that the Killer Whale is a more important predator for some populations than previously believed. Not all behavioural interactions between Killer Whales and other marine mammal species result in predation, however. Some involve 'harassment' by the Killer Whales, feeding by both species in the same area, porpoises playing around Killer Whales, both species apparently 'ignoring' each other, and even apparently unprovoked attacks on Killer Whales by sea lions. These non-predatory interactions are relatively common. We conclude that interactions between Killer Whales and marine mammals are complex, involving many different factors that we are just beginning to understand.     

Local root status: a neglected bio-factor that regulates the home-field advantage of leaf litter decomposition

Background and aims

Bacterial Non-Specific Acid Phosphatase (NSAP) enzymes are capable of dephosphorylating diverse organic phosphoesters but are rarely studied: their distribution in natural and managed environments is poorly understood. The aim of this study was to generate new insight into the environmental distribution of NSAPs and establish their potential global relevance to cycling of organic phosphorus.

Methods

We employed bioinformatic tools to determine NSAP diversity and subcellular localization in microbial genomes; used the corresponding NSAP gene sequences to census metagenomes from diverse ecosystems; studied the effect of long-term land management upon NSAP diversity and abundance.

Results

Periplasmic class B NSAPs are poorly represented in marine and terrestrial environments, reflecting their association with enteric and pathogenic bacteria. Periplasmic class A and outer membrane-associated class C NSAPs are cosmopolitan. NSAPs are more abundant in marine than terrestrial ecosystems and class C more abundant than class A genes, except in an acidic peat where class A genes dominate. A clear effect of land management upon gene abundance was identified.

Conclusions

NSAP genes are cosmopolitan. Class C genes are more widely distributed: their association with the outer-membrane of cells gives them a clear role in the cycling of organic phosphorus, particularly in soils.

     

Resveratrol induces insulin gene expression in mouse pancreatic α-cells

Background

Type 1 and type 2 diabetes are characterized by loss of β-cells; therefore, β-cell regeneration has become one of the primary approaches to diabetes therapy. Resveratrol, a naturally occurring polyphenolic compound, has been shown to improve glycaemic control in diabetic patients, but its action on pancreatic α-cells is not well understood.

Findings

Using mouse α-cells (αTC9), we showed that resveratrol induces expression of pancreatic β-cell genes such as Pdx1 and Ins2 in a SirT1-dependent manner. The mRNA and protein levels of insulin were further increased by histone deacetylase (HDAC) inhibition.

Conclusion

In summary, we provide new mechanistic insight into the anti-diabetic action of resveratrol through its ability to express β-cell genes in α-cells.

     

In-Water Bridge Construction Effects on Manatees with Implications for Marine Megafauna Species

Globally, increasing coastal development requires construction and maintenance of transportation infrastructure that affects terrestrial and aquatic ecosystems. Construction of bridges as part of transportation networks introduces a series of risks to aquatic species near construction zones. We reviewed relevant literature and obtained exemplary case studies to synthesize potential effects of bridge construction on the West Indian manatee (Trichechus manatus), a nearshore megafauna species vulnerable to human activities. Stages of bridge construction including dredging, pile driving, and installation and assembly of bridge components each involve potential direct and indirect effects on manatees. Direct effects such as vessel interactions, entanglement or ingestion, and entrainment may result in acute physical injury or mortality. Indirect effects from construction such as habitat obstruction or degradation and increased noise from construction activities can alter behavior and intraspecies communication and reduce access to essential resources. Some effects of construction may be immediately difficult to quantify, but cumulative effects through time can result in major habitat and species loss. To prevent large-scale negative effects of construction on manatees and other aquatic species, use and evaluation of mitigation strategies should be implemented pre-, during, and post-construction. As the global human population increasingly occupies coastal zones, effective planning of coastal development, including bridge and other in-water construction, will be essential to support conservation and recovery efforts for manatees and other species at risk in these areas. © 2021 The Wildlife Society.