How closely do measures of mitochondrial DNA control region diversity reflect recent trajectories of population decline in birds?

Monitoring levels of genetic diversity in wildlife species is important for understanding population status and trajectory. Knowledge of the distribution and level of genetic diversity in a population is essential to inform conservation management, and help alleviate detrimental genetic impacts associated with recent population bottlenecking. Mitochondrial DNA (mtDNA) markers such as the control region have become a common means of surveying for within-population genetic diversity and detecting signatures of recent population decline. Nevertheless, little attention has been given to examining the mtDNA control region’s sensitivity and performance at detecting instances of population decline. We review genetic studies of bird populations published since 1993 that have used the mtDNA control region and reported haplotype diversity, number of haplotypes and nucleotide diversity as measures of within-population variability. We examined the extent to which these measures reflect differences in known demographic parameters such as current population size, severity of any recent bottleneck and IUCN Red List status. Overall, significant relationships were observed between two measures of genetic diversity (haplotype diversity and the number of haplotypes), and population size across a number of comparisons. Both measures gave a more accurate reflection of recent population history in comparison to nucleotide diversity, for which no significant associations were found. Importantly, levels of diversity only correlated with demographic declines where population sizes were known to have fallen below 500 individuals. This finding suggests that measures of mtDNA control region diversity should be used with a degree of caution when inferring demographic history, particularly bottleneck events at population sizes above N = 500.     

Sex ratio variation and mixed pairs in roe deer: evidence for control of sex allocation?

Sex allocation has provided rich ground for the development of evolutionary theory. The dominant models in vertebrates have provided predictions of sex ratio based on asymmetry in variance in breeding success between sexes in the breeding system, and the relative effect of local competition. In ungulates, empirical work has provided some support for these models, but has also generated apparently contradictory observations. Recent models have provided some predictions for both individual and population sex ratio, showing that the availability of high-quality habitat patches and dispersal rates can critically affect both population- and individual-level expectations. We explore patterns in offspring sex ratio among a large sample of roe deer, a species with some interesting aspects of the breeding system. We found that in singleton pregnancies (the minority) there was an excess of male embryos, which was more marked in does in good condition at most sites. While the sex ratio among twins was close to parity, and unaffected either by average condition among populations or by individual condition within populations, we observed a clear excess of mixed pregnancies (sub-binomial variance, SBV). The excess was greater where the average condition was high. Within sites, population changes in average condition were associated with changes in SBV: in populations declining in condition, SBV also declined. There was no tendency for mixed twins to be more likely in individuals in better condition within a population. We conclude that condition-dependent allocation of sex does occur in roe deer. We suggest that in these "income breeders", mixed pairs might offer the greatest opportunity to optimize maternal investment during lactation, when conditions will be unpredictable, and that this is increasingly the case when average condition is poor.     

Seasonal variation in the population growth rate of a dominant zooplankter: what determines its population dynamics?

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Ranging behaviour of roe deer in an experimental high-density population: Are females territorial?

We studied the ranging behaviour and spatial relationships between seven roe deer during more than 4 years in a partly wooded 14.2-ha enclosure. The animals (three young males, four adult females) were monitored with GPS telemetry collars. As expected, the surface area and overlap of the males’ bimonthly ranges decreased, and the distance between their arithmetic centres increased, as they became adult and, for two of them, territorial. Unexpectedly, females also tended to space out, the surface area and overlap of their bimonthly ranges being minimal in May to June, i.e. during the birth period. The distance between their arithmetic centres reached its maximum at the same time. Overlap between females’ ranges was consistently lower than those between males and females’ ranges, or between 1-year old males’ ranges. Our results raise the questions of female seasonal territoriality and of independence of the spacing systems of the two sexes in roe deer.     

Is there direct and delayed density dependent variation in population structure in a temperate European cyclic vole population?

Population structure, in terms of the body mass, condition, sex and reproductive status of individuals, has been found to vary in phase with population density in cyclic populations of microtine rodents. Because sustained population cycles involve delayed density dependent changes in the population growth rate, we would expect at least some life history traits also to depend on past densities. Detailed, long-term studies of changes in vole life history traits are however few, and are largely restricted to northern Europe. In view of the uncertainty as to whether the cyclic microtine populations of western Europe represent the same phenomenon as those of northern Europe, we studied temporal variation in the structure of a clearly cyclic population of the common vole Microtus arvalis Pallas, in the cereal plains of mid-western France. Our data set contains seasonal, individual-level data from long-term, large-scale trapping covering four entire population cycles. We found considerable cyclic variation in population structure in spring (April), but less so in summer (June). In spring of post-peak years, animals were of low body weight and body condition (particularly females), litter sizes were smaller and there was a reduction in the proportion of breeders. All of these could be proximal drivers of increased mortality rates, or decreased birth rates, contributing to the population declines. Few life history traits, however, showed direct density dependent variation, and none of the traits studied here showed delayed density dependence. We have shown declines in the fecundity and body condition of voles from a western European population that coincides with, and may be a proximal cause of, cyclic declines in population density. Closer attention to proximal causes, by which ecological processes drive cycles, could clarify the extent to which microtine cycles across Europe represent a single phenomenon.     

Establishment of a coastal fish in the Azores: recent colonisation or sudden expansion of an ancient relict population?

The processes and timescales associated with ocean-wide changes in the distribution of marine species have intrigued biologists since Darwin''s earliest insights into biogeography. The Azores, a mid-Atlantic volcanic archipelago located >1000 km off the European continental shelf, offers ideal opportunities to investigate phylogeographic colonisation scenarios. The benthopelagic sparid fish known as the common two-banded seabream (Diplodus vulgaris) is now relatively common along the coastline of the Azores archipelago, but was virtually absent before the 1990s. We employed a multiple genetic marker approach to test whether the successful establishment of the Azorean population derives from a recent colonisation from western continental/island populations or from the demographic explosion of an ancient relict population. Results from nuclear and mtDNA sequences show that all Atlantic and Mediterranean populations belong to the same phylogroup, though microsatellite data indicate significant genetic divergence between the Azorean sample and all other locations, as well as among Macaronesian, western Iberian and Mediterranean regions. The results from Approximate Bayesian Computation indicate that D. vulgaris has likely inhabited the Azores for ∼40 (95% confidence interval (CI): 5.5–83.6) to 52 (95% CI: 6.32–89.0) generations, corresponding to roughly 80–150 years, suggesting near-contemporary colonisation, followed by a more recent demographic expansion that could have been facilitated by changing climate conditions. Moreover, the lack of previous records of this species over the past century, together with the absence of lineage separation and the presence of relatively few private alleles, do not exclude the possibility of an even more recent colonisation event.     

Lagged Population Growth in a Termite Host Colony: Cause or Consequence of Inquilinism?

The presence of foreign organisms in the colonies of social insects could affect energy allocation to growth and reproduction of these hosts. Highly specialized invaders of such long-lived hosts, however, can be selected to be less harmful. After all, it pays for these symbionts to keep their host’s good health thereby prolonging cohabitation in the homeostatic environment of the termite colony. Here, we investigated such a hypothesis, focusing on populational parameters of a termite host sharing its nest with an obligatory termite inquiline. To this end, 19 natural colonies of Constrictotermes cyphergaster (Silvestri, 1901) (Termitidae: Nasutitermitinae) were sampled and the (i) number of individuals, (ii) proportion of soldier/workers in the colonies, and (iii) presence/absence of obligatory inquiline Inquilinitermes microcerus (Silvestri, 1901) (Termitidae: Termitinae) were measured. Results revealed a negative correlation between the number of individuals and the proportion of soldier/workers in the host colonies with the presence of I. microcerus colonies. In search of causal mechanisms for such a correlation, we inspected life history traits of both, inquilines and hosts, hypothesizing that such a result could indicate either (i) a dampening effect of the inquiline upon its host population or (ii) the coincidence of the moment of inquiline infiltration with the natural reduction of C. cyphergaster populational growth at the onset of its reproductive phase.     

Lack of mitochondrial genetic structure in hamlets (Hypoplectrus spp.): recent speciation or ongoing hybridization?

Species in the genus Hypoplectrus (hamlet fish) have been recognized primarily on the basis of colour morphology, which varies substantially. Limited differentiation in other morphological characters, however, has led to ongoing debate about their taxonomy. Our analysis of mtDNA sequences demonstrates neither reciprocal monophyly nor significant genetic differentiation among hamlet colour morphs. These data are potentially consistent with a model of recent speciation due to sexual selection on colour morphology. The presence within hamlets of two divergent mtDNA clades, however, suggests a longer history during which hybridization and gene flow have prevented the differentiation of hamlet colour morphs, at least in neutral genetic markers.     

The ghost of a recent invasion in the reduced feeding rates of spitting cobras during the dry season in a rainforest region of tropical Africa?

Two species of cobras (Naja melanoleuca and Naja nigricollis) are known to occur in south eastern Nigeria, where much of the pristine rainforest surface has been felled in the last thirty years, and where the actual landscape is generally constituted by a mosaic of farmlands, plantations, suburban areas, with a few remnant forest fragments. In this region, Naja nigricollis is currently extending its range, especially by exploiting recently deforested areas. Based on the known general distribution range of this species and on the available literature data, it appears that Naja nigricollis has been colonizing the forested region of south eastern Nigeria, starting from the relatively arid savannas of central Nigeria, where this species aestivates during the driest months. In the forest region, however, snakes do not need to aestivate during the dry season. Nevertheless, whereas Naja melanoleuca has a foraging activity extended all-the-year round, Naja nigricollis reduces feeding rates during the dry months, although it does not suspend above-ground activity in these months. I suggest that rainforest spitting cobras suspend feeding during the dry months because their behaviour is just a ‘ghost’ of their recent past, when they were ‘normal’ spitting cobras of dry savana regions, which were thus constrained to aestivate during the dry season as it is the rule in this species in central and northern Nigeria. The ‘gost-of-the-past hypothesis’ seems to fit well with the ‘invading’ presence of Naja nigricollis in Nigerian areas where they were reported as rare or, even, absent, up to a few decades ago. Other hypotheses are discussed, and rejected.     

Facultative primary sex ratio variation: a lack of evidence in birds?

The facultative control of primary sex ratio by breeding birds has become a major focus in evolutionary biology in recent years. A combination of well-developed theoretical literature and rapid publication of empirical results has created considerable confusion, with controversial claims for both extreme control of primary sex ratio versus no control around inherent random variability. We present a robust and quantitative summary of published empirical literature to assess clearly the body of evidence for female birds to control sex assignment in their offspring. Our meta-analytical approach reveals that published studies do not exhibit any variability beyond that which could be expected owing to sampling error. Therefore, we conclude that facultative control of offspring sex is not a characteristic biological phenomenon in breeding birds.     

Latitudinal Diversity Gradients in New World Bats: Are They a Consequence of Niche Conservatism?

The increase in species diversity from the Poles to the Equator is a major biogeographic pattern, but the mechanisms underlying it remain obscure. Our aim is to contribute to their clarification by describing the latitudinal gradients in species richness and in evolutionary age of species of New World bats, and testing if those patterns may be explained by the niche conservatism hypothesis. Maps of species ranges were used to estimate species richness in a 100 x 100 km grid. Root distances in a molecular phylogeny were used as a proxy for the age of species, and the mean root distance of the species in each cell of the grid was estimated. Generalised additive models were used to relate latitude with both species richness and mean root distance. This was done for each of the three most specious bat families and for all Chiroptera combined. Species richness increases towards the Equator in the whole of the Chiroptera and in the Phyllostomidae and Molossidae, families that radiated in the tropics, but the opposite trend is observed in the Vespertilionidae, which has a presumed temperate origin. In the whole of the Chiroptera, and in the three main families, there were more basal species in the higher latitudes, and more derived species in tropical areas. In general, our results were not consistent with the predictions of niche conservatism. Tropical niche conservatism seems to keep bat clades of tropical origin from colonizing temperate zones, as they lack adaptations to survive cold winters, such as the capacity to hibernate. However, the lower diversity of Vespertilionidae in the Neotropics is better explained by competition with a diverse pre-existing community of bats than by niche conservatism.     

Genetics of recent habitat contraction and reduction in population size: does isolation by distance matter?

Fragmentation and loss of natural habitats are recognized as major threats to contemporary flora and fauna. Detecting past or current reductions in population size is therefore a major aim in conservation genetics. Statistical methods developed to this purpose have tended to ignore the effects of spatial population structure. However in many species, individual dispersal is restricted in space and fine-scale spatial structure such as isolation by distance (IBD) is commonly observed in continuous populations. Using a simulation-based approach, we investigated how comparative and single-point methods, traditionally used in a Wright-Fisher (WF) population context for detecting population size reduction, behave for IBD populations. We found that a complex 'quartet' of factors was acting that includes restricted dispersal, population size (i.e. habitat size), demographic history, and sampling scale. After habitat reduction, IBD populations were characterized by a stronger inertia in the loss of genetic diversity than WF populations. This inertia increases with the strength of IBD, and decreases when the sampling scale increases. Depending on the method used to detect a population size reduction, a local sampling can be more informative than a sample scaled to habitat size or vice versa. However, IBD structure led in numerous cases to incorrect inferences on population demographic history. The reanalysis of a real microsatellite data set of skink populations from fragmented and intact rainforest habitats confirmed most of our simulation results.     

Pioneer neurons: a basis or bottleneck of diversity of nervous systems of Lophotrochozoa?

In a case study on development of larvae of Trochozoa species of different systematic positions, it was shown that peripheral neurons differentiated firstly. According to the characters of early peripheral neurons, in particular their localization in parts that differed from known zones of appearance of central ganglia, the difficult periphery of processes used as a "frame" by differentiated neurons of definitive nervous system, and transient expression of specific markers, it is reputed that these cells are pioneer. On the one hand, pioneer neurons are the bottleneck of morphogenesis diversity in late stages of development which prepare, in early larvae, the framework of the further central nervous system. On the other hand, navigation and marking using pioneer neurons can be a mechanism of evolutionary lability of definitive neural structures. Functional adaptive significance of pioneer neurons of larvae of Trochozoa animals, probably, is in the maintenance of a fast change from larvae life-form to adult life-form in metamorphosis that decreases the time of animals at intermediate stages of morphogenesis, which are associated with a dramatic fall in adaptation.     

Does polyandry control population sex ratio via regulation of a selfish gene?

The extent of female multiple mating (polyandry) can strongly impact on the intensity of sexual selection, sexual conflict, and the evolution of cooperation and sociality. More subtly, polyandry may protect populations against intragenomic conflicts that result from the invasion of deleterious selfish genetic elements (SGEs). SGEs commonly impair sperm production, and so are likely to be unsuccessful in sperm competition, potentially reducing their transmission in polyandrous populations. Here, we test this prediction in nature. We demonstrate a heritable latitudinal cline in the degree of polyandry in the fruitfly Drosophila pseudoobscura across the USA, with northern population females remating more frequently in both the field and the laboratory. High remating was associated with low frequency of a sex-ratio-distorting meiotic driver in natural populations. In the laboratory, polyandry directly controls the frequency of the driver by undermining its transmission. Hence we suggest that the cline in polyandry represents an important contributor to the cline in sex ratio in nature. Furthermore, as the meiotic driver causes sex ratio bias, variation in polyandry may ultimately determine population sex ratio across the USA, a dramatic impact of female mating decisions. As SGEs are ubiquitous it is likely that the reduction of intragenomic conflict by polyandry is widespread.     

Can a seed bank maintain the genetic variation in the above ground plant population?

There are indications that a persistent seed bank can protect small and isolated plant populations from local extinction. Genetic mechanisms contributing to this phenomenon are the increase of local effective population size – and hence the decrease of genetic drift – through a reservoir of persistent seeds, and the accumulation of intergenerational genetic diversity in the seed bank. To find evidence for these mechanisms, we conducted two formal meta-analyses. First, we analyzed 42 published habitat fragmentation studies and investigated whether the degree of genetic differentiation between fragmented plant populations was mediated by seed longevity. Second, we reviewed 13 published studies reporting the genetic diversity of both the seed bank and the above ground plants, aiming at comparing genetic diversity contained in the seed bank with the above ground vegetation. We conclude that a persistent seed bank may indeed mitigate the consequences of habitat fragmentation and protect a species from genetic drift and population genetic differentiation. We found no evidence, however, of high levels of genetic diversity accumulating in the soil seed bank. If genetic differences are present between the standing crop and the seed bank, they are very likely the result of local selection acting either directly or indirectly as a filter on the alleles present in the seed bank. We finally suggest that 1) the role of the seed bank should not be neglected in habitat fragmentation studies and 2) it is not very fruitful to continue comparing seed bank genetic diversity with above ground plant genetic diversity, unless this is performed under different selection regimes.     

Lack of replication of interactions between polymorphisms in rheumatoid arthritis susceptibility: case–control study

Introduction

Approximately 100 loci have been definitively associated with rheumatoid arthritis (RA) susceptibility. However, they explain only a fraction of RA heritability. Interactions between polymorphisms could explain part of the remaining heritability. Multiple interactions have been reported, but only the shared epitope (SE) × protein tyrosine phosphatase nonreceptor type 22 (PTPN22) interaction has been replicated convincingly. Two recent studies deserve attention because of their quality, including their replication in a second sample collection. In one of them, researchers identified interactions between PTPN22 and seven single-nucleotide polymorphisms (SNPs). The other showed interactions between the SE and the null genotype of glutathione S-transferase Mu 1 (GSTM1) in the anti–cyclic citrullinated peptide–positive (anti-CCP⁺) patients. In the present study, we aimed to replicate association with RA susceptibility of interactions described in these two high-quality studies.

Methods

A total of 1,744 patients with RA and 1,650 healthy controls of Spanish ancestry were studied. Polymorphisms were genotyped by single-base extension. SE genotypes of 736 patients were available from previous studies. Interaction analysis was done using multiple methods, including those originally reported and the most powerful methods described.

Results

Genotypes of one of the SNPs (rs4695888) failed quality control tests. The call rate for the other eight polymorphisms was 99.9%. The frequencies of the polymorphisms were similar in RA patients and controls, except for PTPN22 SNP. None of the interactions between PTPN22 SNPs and the six SNPs that met quality control tests was replicated as a significant interaction term—the originally reported finding—or with any of the other methods. Nor was the interaction between GSTM1 and the SE replicated as a departure from additivity in anti-CCP⁺ patients or with any of the other methods.

Conclusions

None of the interactions tested were replicated in spite of sufficient power and assessment with different assays. These negative results indicate that whether interactions are significant contributors to RA susceptibility remains unknown and that strict standards need to be applied to claim that an interaction exists.