Evolutionary changes of Hox genes and relevant regulatory factors provide novel insights into mammalian morphological modifications

The diversity of body plans of mammals accelerates the innovation of lifestyles and the extensive adaptation to different habitats, including terrestrial, aerial and aquatic habitats. However, the genetic basis of those phenotypic modifications, which have occurred during mammalian evolution, remains poorly explored. In the present study, we synthetically surveyed the evolutionary pattern of Hox clusters that played a powerful role in the morphogenesis along the head–tail axis of animal embryos and the main regulatory factors (Mll, Bmi1 and E2f6) that control the expression of Hox genes. A deflected density of repetitive elements and lineage‐specific radical mutations of Mll have been determined in marine mammals with morphological changes, suggesting that evolutionary changes may alter Hox gene expression in these lineages, leading to the morphological modification of these lineages. Although no positive selection was detected at certain ancestor nodes of lineages, the increased ω values of Hox genes implied the relaxation of functional constraints of these genes during the mammalian evolutionary process. More importantly, 49 positively‐selected sites were identified in mammalian lineages with phenotypic modifications, indicating adaptive evolution acting on Hox genes and regulatory factors. In addition, 3 parallel amino acid substitutions in some Hox genes were examined in marine mammals, which might be responsible for their streamlined body.     

Adaptive evolutionary expansion of the ribonuclease 6 in Rodentia

Ribonuclease 6 (RNase6 or RNase K6) is a protein that belongs to a superfamily thought to be the sole verte‐brate‐specific enzyme known for a wide range of physiological functions, including digestion, cytotoxicity, angiogenesis, male reproduction and host defense. In our study, 51 functional genes and 11 pseudogenes were identified from 27 Rodentia species. Intriguingly, in the 3 main lineages of rodents there were multiple RNase6s identified in all species of Ctenohystrica, whereas only a single RNase6 was observed in other Rodentia species examined except for 2 species in the mouse‐related clade. The evolutionary scenario of “birth (gene duplication) and death (gene deactivation)” and gene sorting have been demonstrated in Ctenohystrica. In addition, bursts of positive selection, diversification of isoelectric point and positive net charge have been identified in Ctenohystrica, especially at two key sites that are involved in antimicrobial function. Site Trp30 has undergone positive selection and Ile45 has changed into other residues in Group B and Group C of the Ctenohystrica. Our results demonstrated a complex and intriguing evolutionary pattern of rodent RNase6, and indicated that functional modification may have occurred, which establishes an important theoretical foundation for future functional assays in rodent RNase6.     

Narrow versus broad: sexual dimorphism in the wing form of western European species of the subgenus Avaritia (Culicoides,Ceratopogonidae)

While wing form is known to differ between males and females of the genus Culicoides, detailed studies of sexual dimorphism are lacking. In this study, we analyze sex-specific differences in the wing form of 5 species of the subgenus Avaritia, using geometric morphometrics and comparative phylogenetic methods. Our results confirm the existence of marked sexual dimorphism in the wing form of the studied species and reveal for the first time that while there is a shared general pattern of sexual shape dimorphism within the subgenus, sexual size dimorphism, and particular features of sexual shape dimorphism differ among species. Sexual shape dimorphism was found to be poorly associated to size and the evolutionary history of the species. The tight association of sexual shape dimorphism with aspect ratio suggests that the shape of the wing is optimized for the type of flight of each sex, that is, dispersal flight in females versus aerobatic flight in males. Moreover, the fact that interspecific shape differences are greater and more strongly associated to aspect ratio in males than in females might be indicating that in males the selective pressures affecting flight performance characteristics are more heterogeneous and/or stronger than in females among the studied species.     

Sexual size dimorphism in the lizard Oplurus cuvieri cuvieri (Squamata,Opluridae) from Madagascar

Sexual size dimorphism in the medium-sized lizard Oplurus cuvieri cuvieri, which is endemic to the dry deciduous forest of Madagascar, is presented. Adults are sexually dimorphic in body size, head size, and tail length. Males have a greater snout–vent length (SVL), head depth, head width, jaw length, tail length and body mass than females. Juvenile males have greater annual SVL growth rates than juvenile females, contributing to adult sexual size dimorphism. Moreover, the rates of increase in head depth and width differ significantly between the sexes after reaching maturity so that adult males have larger heads for a given body size than adult females. I suggest three proximate mechanisms that may cause sex-related differences in adult head size of O. c. cuvieri based on natural selection; to reduce intersexual food competition, sexual selection involving mate acquisition in males, and ontogenetic change of allometry to improve reproductive output in females.     

Sexual dimorphism in the African legless skink subfamily Acontiinae (Reptilia: Scincidae)

The extent to which sexual dimorphism in snout–vent length, tail length and head shape (length, width and height) manifests itself in the legless fossorial skink subfamily Acontiinae was investigated in representatives of all four of its genera, Acontias, Microacontias, Acontophiops and Typhlosaurus. Where data were available fecundity selection and diet partitioning (ecological causation) were tested as possible proximate causes for dimorphisms found. The possibility of a relationship between head shape and microhabitat density was also investigated. The data showed that significant sexual dimorphism in snout–vent length and head shape was present in only a minority of taxa and that it was absent with respect to tail length. There are indications of a relationship between head shape and microhabitat density, and head shape seems to become increasingly more pointed as SVL increases. A serious impediment to placing the findings of this study into a firm evolutionary context is the general lack of information about the ecology, social organization and behaviour of the taxa.     

Use of high‐density SNP data to identify patterns of diversity and signatures of selection in broiler chickens

The development of broiler chickens over the last 70 years has been accompanied by large phenotypic changes, so that the resulting genomic signatures of selection should be detectable by current statistical techniques with sufficiently dense genetic markers. Using two approaches, this study analysed high‐density SNP data from a broiler chicken line to detect low‐diversity genomic regions characteristic of past selection. Seven regions with zero diversity were identified across the genome. Most of these were very small and did not contain many genes. In addition, fifteen regions were identified with diversity increasing asymptotically from a low level. These regions were larger and thus generally included more genes. Several candidate genes for broiler traits were found within these ‘regression regions’, including IGF1, GPD2 and MTNR1AI. The results suggest that the identification of zero‐diversity regions is too restrictive for characterizing regions under selection, but that regions showing patterns of diversity along the chromosome that are consistent with selective sweeps contain a number of genes that are functional candidates for involvement in broiler development. Many regions identified in this study overlap or are close to regions identified in layer chicken populations, possibly due to their shared precommercialization history or to shared selection pressures between broilers and layers.     

Reproductive strategies in males of the world's southernmost lizards

Reproductive and life history patterns in reptiles are tightly related to the environmental conditions, so male reproductive cycles have been historically characterized as continuous, for tropical lizards, or seasonal, for temperate lizards. However, males of Liolaemus and Phymaturus lizards (Liolaemidae), from cold temperate climates of high altitudes or latitudes in Argentina and Chile, have developed a variety of reproductive cycles to coordinate with the short female reproductive season and to deal with the low frequency of reproductive females in the population. Using gonadal histology and morphological analysis, we describe the male reproductive biology, fat storage and sexual dimorphism of the viviparous lizards Liolaemus sarmientoi and Liolaemus magellanicus that inhabit an austral grass steppe at 51°S, in the southern limit of the American continent. Males of L. sarmientoi and L. magellanicus are reproductively available during the entire activity season of approximately 5 months. In addition, males of both species exhibit greater body sizes than females in morphological variables relevant in sexual selection. Meanwhile, females of both species exhibit larger inter‐limb length than conspecific males, which suggests fecundity selection to increase space for a larger litter size. The continuous sperm production throughout the activity season allows these liolaemids to mate at any time when females ovulate, representing a selective advantage to deal with the short activity season and the adversities of the cold environment they inhabit.     

Sexual dimorphism in two girdled lizard species,Cordylus niger and Cordylus cordylus

The extent of sexual selection in two girdled lizard species was evaluated by measuring sexual dimorphism in those characters normally affected by sexual selection. Neither Cordylus niger, a cool-adapted species, nor C. cordylus, a warm-adapted species, displayed any notable sexual differences in asymptotic body sizes, but both species displayed slight dimorphism in head size measurements. The C. niger sample contained more large males than large females, which may be attributed to a lower growth rate in females. In the cool Saldanha area, females of both species lack generation glands. In the warmer Gansbaai area, these glands are present in females of C. cordylus, but in lower numbers than in males. Sex ratios favouring females, have been recorded for both species. The observed sexual dimorphism in the two species seems to be mainly the result of differential energy allocation by females, and not of sexual selection perse.     

Immune challenge of mating effort: steroid hormone profile,dark ventral patch and parasite burden in relation to intrasexual competition in male Iberian red deer

Testosterone secretion may regulate the reproductive effort and the development of sexual traits, but it may also involve costs at the immunological and metabolic levels. However, the evidence for this trade‐off in wild populations is scarce. Cortisol also plays an important role in mediating the reproductive and immune functions. In this study, we analyzed whether the endoparasite burden relates to hormonal levels (fecal testosterone and cortisol metabolites) and/or morphological sexual traits (size of the dark ventral patch, a trait that indicates reproductive effort in males) in male Iberian red deer. For this purpose, we sampled male red deer harvested during hunting actions in 2 types of populations in south western Spain that differed in structure, affecting the level of male–male competition for mates. We used coprological analyses to estimate the parasite burden mainly of gastrointestinal and bronchopulmonary nematodes and of protozoa, and assessed testosterone and cortisol metabolite levels from fecal pellets. We found a positive relationship of host parasitation with both testosterone levels and the size of the dark ventral patch, but these relationships depended on the intensity of male–male competition in the population, being only found under the high‐competition scenario. These results are discussed under the hypothesis of the testosterone immunocompetence handicap, suggesting a cost at the immunological level, and, therefore, higher susceptibility to parasite infection in males that make a greater reproductive effort. However, this effect seems to be modulated by the social environment (male–male competition) that might lead to different optima in testosterone production and sexual trait development.     

Phylogeography and genetic diversity of Psammophis schokari (Serpentes) in North Africa based on mitochondrial DNA sequences

The snake Psammophis schokari has a widespread distribution across North Africa, and in Morocco/Western Sahara is represented by three different morphotypes: striped, unicoloured and the Western-Sahara morph. ND4 mitochondrial DNA sequences from 28 specimens comprising 20 P. shokari, two P. aegyptius, one P. elegans, two P. sibilans, one P. condanarus and two outgroups were analysed. Within P. schokari we identified four genetic lineages (Morocco/Western Sahara, Mauritania, Algeria and Israel) with a genetic divergence ranging from 4-5%, less than that typically found between different species. Surprisingly, Moroccan/Western Sahara and Algerian lineages are the most divergent ones. This geographic substructuring may be due to severe climate changes in the Sahara desert between the Miocene and Pleistocene associated with expansion/contraction phases of this desert. Psammophis aegyptius is the sister-taxon of Psammophis schokari with a high level of genetic divergence between them (10.7%) supporting the recognition of P. aegyptius as a distinct species. The three Moroccan/Western Sahara colour morphotypes form one genetic lineage, indicating that colour pattern does not reflect a different phylogenetic history, and is probably an ecological adaptation to the local environment.     

新疆塔里木盆地叶城沙蜥的两性异形

叶城沙蜥是一种主要分布于中国新疆南部地区的蜥蜴,通过测量和比较采自新疆塔里木盆地且末县叶城沙蜥的个体大小以及口宽等8个形态特征,研究了叶城沙蜥的两性异形。研究共采集叶城沙蜥62只,其中成年雌性个体27只,雄性个体35只。结果显示:(1)叶城沙蜥雌雄性成体的体长有显著差异,雄性大于雌性,表明叶城沙蜥具有雄性偏大的两性异形模式;(2)叶城沙蜥其他身体形态特征中尾长、腹长和头长3个特征有显著差异,其中雄性的尾长和头长大于雌性,而雌性的腹长大于雄性;(3)叶城沙蜥雌雄性个体间的口宽、眼间距等其他形态特征则没有显著差异。叶城沙蜥的两性异形表现为雄性大于雌性,并且雄性具有更大的头部和更长的尾部,雌性具有更长有腹部,这可能是雄性个体面临的性选择压力与雌性个体面临的繁殖压力共同作用的结果。     

Egg trait variation in a large hawk‐cuckoo (Hierococcyx sparverioides) host population of Chinese babax (Babax lanceolatus)

Mutual interaction between brood parasites and their hosts is a well‐known model system for studying host–parasite coevolution. Both parties have acted reciprocally, resembling an evolutionary arms race, in which adaptations and counter‐adaptations have evolved as a result of host–parasite dynamics, such as the classical cuckoo–host system. Discrimination among parasite and cuckoo eggs and rejection of foreign eggs is regarded as an important anti‐parasitism strategy. The Chinese babax (Babax lanceolatus) is a large hawk‐cuckoo (Hierococcyx sparverioides) host distributed in southwest China. A previous study shows that the babax is an intermediate egg rejector, and most cuckoo eggs are accepted by the Chinese babax, although a small proportion of hosts reject cuckoo eggs. Interestingly, the large hawk‐cuckoo lays non‐mimetic eggs in contrast to the uniform blue eggs of babaxes. Because egg coloration is a critical cue used by host species in favor of the recognition of parasitic eggs by hosts, we used a spectrometer to quantify egg color variation to understand the differentiation in discrimination ability between the egg rejectors and acceptors. We found that the chroma of intra‐clutch variation of babax eggs was more consistent in egg rejectors than in acceptors. However, no statistical significance was found in inter‐clutch variation between these two types of hosts. Our results suggest that hosts lay eggs with a low level of intra‐clutch variation without the necessity of a high level of inter‐clutch variation simultaneously as predicted by the egg signature hypothesis. This study may further indicate that selection pressures from evolutionarily recent parasites can drive individual‐based differences in an anti‐parasitism strategy.     

Elytron length and sexual dimorphism in Zonocerus elegans (Thunb.), (Orthoptera: Pyrgomorphidae)

Adults of the African pyrgomorphid grasshopper, Zonocerus elegans Thunberg, exhibit strong alar polymorphism, especially in the male sex, with wings either vestigial or fully developed. Analysis of body and elytron lengths of about 400 insects revealed sexual dimorphism, females being larger than males, and showed a bimodal distribution for wing length. The difference in average wing length between long-winged and short-winged forms was 14 mm. Since the two distributions (short and long) do not overlap, they would correspond closely to the subsidiary infra-subspecific categories f. brachyptera and f. macroptera, respectively, although even wings of the lower macroptera range seem to be vestigial, i.e. imperfectly developed and useless for flight.     

Identification of Genes Involved in Taura Syndrome Virus Resistance in Litopenaeus Vannamei

Abstract

The goal of the present research was to identify the genes that are differentially expressed between two lineages of Pacific white shrimp Litopenaeus vannamei displaying different susceptibilities to Taura syndrome virus (TSV) and to understand the molecular pathways involved in resistance to the disease. An oligonucleotide microarray was constructed and used to identify several genes that were differentially expressed in the two L. vannamei lineages following infection with TSV. Individual L. vannamei from either resistant or susceptible lineages were exposed via injection to TSV. Individuals were removed at 6 and 24 h postinfection, and gene expression was assessed with the in-house microarray. The microarray data resulted in the selection of a set of 397 genes that were altered by TSV exposure between the different lineages. Significantly differentially expressed genes were subjected to hierarchical clustering and revealed a lineage-dependent clustering at 24 h postinoculation, but not at 6 h postinoculation. Discriminant analysis resulted in the identification of a set of 11 genes that were able to correctly classify Pacific white shrimp as resistant or susceptible based on gene expression data.

Received June 21, 2013; accepted October 24, 2013     

Evidence of multiple divergent mitochondrial lineages within the southern African diplopod genus Bicoxidens Attems, 1928 (Spirostreptida)

Two recent studies have suggested that divergent mitochondrial lineages may be present within spirostreptid genera such as Bicoxidens Attems, 1928. Bicoxidens, similar to many other endemic soil invertebrates, exhibits low dispersal capabilities and strict microclimate habitat preferences, attributes that often lead to geographic isolation. Given that prolonged geographic isolation often lays the foundation for population genetic differentiation, genetic divergence and possibly speciation, there was good reason to suspect that Bicoxidens may consist of several distinct lineages. On this basis, the mitochondrial cytochrome c oxidase subunit 1 (COI) was used to reconstruct the phylogeny of Bicoxidens and reveal divergent lineages within the genus. Maximum likelihood and Bayesian inference analyses recovered a paraphyletic Bicoxidens phylogram with divergent lineages present in three species – B. friendi, B. flavicollis and B. brincki – suggesting high genetic diversity within the genus. Bayesian genetic cluster analyses suggested the presence of multiple distinct mitochondrial lineages within the genus with four identified in B. flavicollis alone. It was therefore concluded that the divergent lineages observed among Bicoxidens populations may suggest the presence of hidden species.     

Phylogenetic tests of a Cercopithecus monkey hybrid reveal X-chromosomal polyphyly of C. cephus and emerging patterns in the cephus species group radiation

A captive Cercopithecus nictitans × C. cephus male was examined at loci on the X- and Y-chromosomes as a test of previously described phylogenetic methods for identifying hybrid Cercopithecus monkeys. The results confirm the reliability of such assays, indicating that they can be of immediate utility for studies of wild populations in Gabon, where the two species have hybridised. A closer examination of the resultant sex chromosomal topologies, combined with recent mitochondrial studies, reveals two emerging patterns in the evolution of the cephus species group. First, all three genetic systems (X-DNA, Y-DNA and mtDNA) agree that the earliest divergence separates West African from Central African species, consistent with a major faunal transition zone in the vicinity of the Cross River. Second, the X-DNA and mtDNA trees reveal polyphyly of C. cephus lineages. It is unclear at present whether these polyphylies are due to ancestral hybridisation or incomplete lineage sorting, or both.     

Mitochondrial DNA variation and genetic relationships in Spanish donkey breeds (Equus asinus)

In this study, the mitochondrial DNA diversity of six Spanish donkey breeds and two African donkey populations (one from Morocco and the other from Zimbabwe) was analysed. A total of 79 animals were sequenced for 313 bp of the cytochrome b gene, and 91 individuals for 383 bp of the D‐loop region or control‐region. Sequence comparisons and phylogenetic analyses of both Spanish and African populations revealed low diversity. Only six and seven haplotypes respectively were found in cytochrome b and the D‐loop region. Relatively low nucleotide diversity (π) values were detected in these populations. The π values, from the D‐loop region, ranged from 0.0006 to 0.0169 for the Catalana and Andaluza breeds, respectively. The obtained results seem to confirm the existence of two divergent maternal lineages of African origin (Equus asinus africanus and E. a. somaliensis). In this paper the genetic relationships between these breeds are analysed and compared with those obtained in other European populations. Also, the data on the genetic relationships between the populations, obtained from nuclear DNA (microsatellites) and mitochondrial DNA (cytochrome b and D‐loop region) is argued and interpreted.     

Lineage diversification and niche evolution in the Reeves’ Butterfly Lizard Leiolepis reevesii (Agamidae)

We used mitochondrial cytochrome b and ND4 genes and 9 microsatellite loci to determine genetic diversity, population structure, evolutionary history, and migration patterns within the Reeves’ butterfly lizard Leiolepis reevesii (Agamidae). Considering molecular-based phylogeographical lineages, we then performed niche equivalency and similarity tests between divergent lineages. Phylogenetic analyses based on mitochondrial DNA (mtDNA) data revealed 2 lineages (A and B) diverging ≈0.84 million years ago and, respectively, restricted to the northern and southern portions of the Wuzhishan and Yinggeling mountain ranges. Lineage B contains individuals from southern Hainan; Lineage A includes individuals from all other localities and can be further divided into 3 clusters according to microsatellite data. The null hypothesis that the 2 lineages shared identical niches was rejected in all niche equivalency tests, indicating niche shifts during genetic divergence. Similarity tests provided evidence of niche conservatism, suggesting that the 2 lineages share more characteristics of their niche spaces than randomly expected. The niche similarity and equivalency tests indicated a complex niche pattern in which both lineages share a main portion of their ecological spaces. The climatic niche of Lineage B represented a marginal and specialized fraction of the entire ecological space of the climatic niche of Lineage A, with warmer conditions. Isolation caused by orogenesis and subsequent niche divergence, together with local adaptation, may have led to genetic differentiation and further lineage sorting in L. reevesii.     

Epistatic interactions between pterin and carotenoid genes modulate intra-morph color variation in a lizard

Color polymorphisms have become a major topic in evolutionary biology and substantial efforts have been devoted to the understanding of the mechanisms responsible for originating such colorful systems. Within-morph continuous variation, on the other hand, has been neglected in most of the studies. Here, we combine spectrophotometric/visual modeling and genetic data to study the mechanisms promoting continuous variation within categorical color morphs of Podarcis muralis. Our results suggest that intra-morph variability in the pterin-based orange morph is greater compared to white and yellow morphs. We also show that continuous variation within the orange morph is partially discriminable by conspecifics. Genotyping results indicate that allelic variants at the BCO2 locus (responsible for deposition of yellow carotenoids) contribute to generate continuous variation in orange individuals. However, other intrinsic and/or extrinsic mechanisms, such as body size, might be involved, opening a new avenue for future research on the drivers of continuous variation within-morphs.     

Aspects of reproduction in female Bos indicus cattle: a review

SUMMARY Differences occur between female Bos indicus and Bos taurus cattle in various aspects of reproductive physiology and behaviour. These may be associated with different natural and human selection pressures, compounded by strong genotype-environment interactions. B indicus cattle are better adapted for tropical environments (despite overall poor cattle reproductive rates in these regions) which tend to be more stressful for B taurus genotypes. Conversely, B taurus cattle generally show superior reproductive and productive traits under more favoured, temperate conditions. Despite genotype-environment effects, B indicus females are generally considered to take longer to achieve puberty and to have longer gestation lengths, exhibit prolonged postpartum anoestrus, show greater seasonality of reproductive traits (tending to be long-day breeders), display a shorter, less overt oestrus as well as less tendency to allow riding behaviour by subordinate females. Some groups appear to have increased losses both during pregnancy and in the neonatal period. On the positive side, B indicus females respond well to managerial and nutritional interventions, tend to have greater reproductive longevity and they generally exhibit strong maternal traits. Culling of infertile females and selection for greater male scrotal circumference and sex-drive, in conjunction with the use of target weights, body condition scoring and weaning stratagems can improve reproductive rates in B indicus females.