The Evolution of Male-Biased Dispersal under the Joint Selective Forces of Inbreeding Load and Demographic and Environmental Stochasticity

Peer reviewed

The effects of habitat fragmentation on the demography and population genetic structure of Uromys Caudimaculatus

Habitat fragmentation can have an impact on a wide variety of biological processes including abundance, life history strategies, mating system, inbreeding and genetic diversity levels of individual species. Although fragmented populations have received much attention, ecological and genetic responses of species to fragmentation have still not been fully resolved. The current study investigated the ecological factors that may influence the demographic and genetic structure of the giant white-tailed rat (Uromys caudimaculatus) within fragmented tropical rainforests. It is the first study to examine relationships between food resources, vegetation attributes and Uromys demography in a quantitative manner. Giant white-tailed rat densities were strongly correlated with specific suites of food resources rather than forest structure or other factors linked to fragmentation (i.e. fragment size). Several demographic parameters including the density of resident adults and juvenile recruitment showed similar patterns. Although data were limited, high quality food resources appear to initiate breeding in female Uromys. Where data were sufficient, influx of juveniles was significantly related to the density of high quality food resources that had fallen in the previous three months. Thus, availability of high quality food resources appear to be more important than either vegetation structure or fragment size in influencing giant white-tailed rat demography. These results support the suggestion that a species’ response to fragmentation can be related to their specific habitat requirements and can vary in response to local ecological conditions. In contrast to demographic data, genetic data revealed a significant negative effect of habitat fragmentation on genetic diversity and effective population size in U. caudimaculatus. All three fragments showed lower levels of allelic richness, number of private alleles and expected heterozygosity compared with the unfragmented continuous rainforest site. Populations at all sites were significantly differentiated, suggesting restricted among population gene flow. The combined effects of reduced genetic diversity, lower effective population size and restricted gene flow suggest that long-term viability of small fragmented populations may be at risk, unless effective management is employed in the future. A diverse range of genetic reproductive behaviours and sex-biased dispersal patterns were evident within U. caudimaculatus populations. Genetic paternity analyses revealed that the major mating system in U. caudimaculatus appeared to be polygyny at sites P1, P3 and C1. Evidence of genetic monogamy, however, was also found in the three fragmented sites, and was the dominant mating system in the remaining low density, small fragment (P2). High variability in reproductive skew and reproductive success was also found but was less pronounced when only resident Uromys were considered. Male body condition predicted which males sired offspring, however, neither body condition nor heterozygosity levels were accurate predictors of the number of offspring assigned to individual males or females. Genetic spatial autocorrelation analyses provided evidence for increased philopatry among females at site P1, but increased philopatry among males at site P3. This suggests that male-biased dispersal occurs at site P1 and female-biased dispersal at site P3, implying that in addition to mating systems, Uromys may also be able to adjust their dispersal behaviour to suit local ecological conditions. This study highlights the importance of examining the mechanisms that underlie population-level responses to habitat fragmentation using a combined ecological and genetic approach. The ecological data suggested that habitat quality (i.e. high quality food resources) rather than habitat quantity (i.e. fragment size) was relatively more important in influencing giant white-tailed rat demographics, at least for the populations studied here . Conversely, genetic data showed strong evidence that Uromys populations were affected adversely by habitat fragmentation and that management of isolated populations may be required for long-term viability of populations within isolated rainforest fragments.

The influence of habitat heterogeneity on patterns of connectivity among rabbit populations in southern Queensland

Patterns of connectivity among local populations influence the dynamics of regional systems, but most ecological models have concentrated on explaining the effect of connectivity on local population structure using dynamic processes covering short spatial and temporal scales. In this study, a model was developed in an extended spatial system to examine the hypothesis that long term connectivity levels among local populations are influenced by the spatial distribution of resources and other habitat factors. The habitat heterogeneity model was applied to local wild rabbit populations in the semi-arid Mitchell region of southern central Queensland (the Eastern system). Species' specific population parameters which were appropriate for the rabbit in this region were used. The model predicted a wide range of long term connectivity levels among sites, ranging from the extreme isolation of some sites to relatively high interaction probabilities for others. The validity of model assumptions was assessed by regressing model output against independent population genetic data, and explained over 80% of the variation in the highly structured genetic data set. Furthermore, the model was robust, explaining a significant proportion of the variation in the genetic data over a wide range of parameters. The performance of the habitat heterogeneity model was further assessed by simulating the widely reported recent range expansion of the wild rabbit into the Mitchell region from the adjacent, panmictic Western rabbit population system. The model explained well the independently determined genetic characteristics of the Eastern system at different hierarchic levels, from site specific differences (for example, fixation of a single allele in the population at one site), to differences between population systems (absence of an allele in the Eastern system which is present in all Western system sites). The model therefore explained the past and long term processes which have led to the formation and maintenance of the highly structured Eastern rabbit population system. Most animals exhibit sex biased dispersal which may influence long term connectivity levels among local populations, and thus the dynamics of regional systems. When appropriate sex specific dispersal characteristics were used, the habitat heterogeneity model predicted substantially different interaction patterns between female-only and combined male and female dispersal scenarios. In the latter case, model output was validated using data from a bi-parentally inherited genetic marker. Again, the model explained over 80% of the variation in the genetic data. The fact that such a large proportion of variability is explained in two genetic data sets provides very good evidence that habitat heterogeneity influences long term connectivity levels among local rabbit populations in the Mitchell region for both males and females. The habitat heterogeneity model thus provides a powerful approach for understanding the large scale processes that shape regional population systems in general. Therefore the model has the potential to be useful as a tool to aid in the management of those systems, whether it be for pest management or conservation purposes.

The X-chromosome and susceptibility to ankylosing spondylitis

Objective. Ankylosing spondylitis (AS) affects 0.25-1.0% of the population, and its etiology is incompletely understood. Susceptibility to this highly familial disease (λ(s) = 58) is primarily genetically determined. There is a significant sex bias in AS, and there are differences in recurrence risk to the offspring of affected mothers and fathers, suggesting that there may be an X-linked recessive effect. We undertook an X- chromosome linkage study to determine any contribution of the X-chromosome to AS susceptibility. Methods. A linkage study of the X-chromosome using 234 affected sibling pairs was performed to investigate this hypothesis. Results. No linkage of the X-chromosome with susceptibility to AS was found. Model- free multipoint linkage analysis strongly excluded any significant genetic contribution (λ ≥1.5) to AS susceptibility encoded on the X-chromosome (logarithm of odds [LOD] <-2.0). Smaller genetic effects (A ≥1.3) were also found to be unlikely (LOD <-1.0). Conclusion. The sex bias in AS is not explained by X-chromosome-encoded genetic effects. The disease model best explaining the sex bias in occurrence and transmission of AS is a polygenic model with a higher susceptibility threshold in females.

Tracing the Origins of Hakka and Chaoshanese by Mitochondrial DNA Analysis

Hakka and Chaoshanese are two unique Han populations residing in southern China but with northern Han (NH) cultural traditions and linguistic influences. Although most of historical records indicate that both populations migrated from northern China in the last two thousand years, no consensus on their origins has been reached so far. To shed more light on the origins of Hakka and Chaoshanese, mitochondrial DNAs (mtDNAs) of 170 Hakka from Meizhou and 102 Chaoshanese from Chaoshan area, Guangdong Province, were analyzed. Our results show that some southern Chinese predominant haplogroups, e.g. B, F, and M7, have relatively high frequencies in both populations. Although median network analyses show that Hakka/Chaoshanese share some haplotypes with NH, interpopulation comparison reveals that both populations show closer affinity with southern Han (SH) populations than with NH. In consideration of previous results from nuclear gene (including Y chromosome) research, it is likely that matrilineal landscapes of both Hakka and Chaoshanese have largely been shaped by the local people during their migration southward and/or later colonization in southern China, and factors such as cultural assimilation, patrilocality, and even sex-bias in the immigrants might have played important roles during the process. Am J Phys Anthropol 141:124-130, 2010. (C) 2009 Wiley-Liss, Inc.

Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate.

BACKGROUND: Like other vertebrates, primates recognize their relatives, primarily to minimize inbreeding, but also to facilitate nepotism. Although associative, social learning is typically credited for discrimination of familiar kin, discrimination of unfamiliar kin remains unexplained. As sex-biased dispersal in long-lived species cannot consistently prevent encounters between unfamiliar kin, inbreeding remains a threat and mechanisms to avoid it beg explanation. Using a molecular approach that combined analyses of biochemical and microsatellite markers in 17 female and 19 male ring-tailed lemurs (Lemur catta), we describe odor-gene covariance to establish the feasibility of olfactory-mediated kin recognition. RESULTS: Despite derivation from different genital glands, labial and scrotal secretions shared about 170 of their respective 338 and 203 semiochemicals. In addition, these semiochemicals encoded information about genetic relatedness within and between the sexes. Although the sexes showed opposite seasonal patterns in signal complexity, the odor profiles of related individuals (whether same-sex or mixed-sex dyads) converged most strongly in the competitive breeding season. Thus, a strong, mutual olfactory signal of genetic relatedness appeared specifically when such information would be crucial for preventing inbreeding. That weaker signals of genetic relatedness might exist year round could provide a mechanism to explain nepotism between unfamiliar kin. CONCLUSION: We suggest that signal convergence between the sexes may reflect strong selective pressures on kin recognition, whereas signal convergence within the sexes may arise as its by-product or function independently to prevent competition between unfamiliar relatives. The link between an individual's genome and its olfactory signals could be mediated by biosynthetic pathways producing polymorphic semiochemicals or by carrier proteins modifying the individual bouquet of olfactory cues. In conclusion, we unveil a possible olfactory mechanism of kin recognition that has specific relevance to understanding inbreeding avoidance and nepotistic behavior observed in free-ranging primates, and broader relevance to understanding the mechanisms of vertebrate olfactory communication.

Duplications of BHLHA9 are associated with ectrodactyly and tibia hemimelia inherited in non-Mendelian fashion

Background Split-hand/foot malformation (SHFM)-also known as ectrodactyly-is a congenital disorder characterised by severe malformations of the distal limbs affecting the central rays of hands and/or feet. A distinct entity termed SHFLD presents with SHFM and long bone deficiency. Mouse models suggest that a defect of the central apical ectodermal ridge leads to the phenotype. Although six different loci/mutations (SHFM1-6) have been associated with SHFM, the underlying cause in a large number of cases is still unresolved. Methods High resolution array comparative genomic hybridisation (CGH) was performed in patients with SHFLD to detect copy number changes. Candidate genes were further evaluated for expression and function during limb development by whole mount in situ hybridisation and morpholino knock-down experiments. Results Array CGH showed microduplications on chromosome 17p13.3, a locus previously associated with SHFLD. Detailed analysis of 17 families revealed that this copy number variation serves as a susceptibility factor for a highly variable phenotype with reduced penetrance, particularly in females. Compared to other known causes for SHFLD 17p duplications appear to be the most frequent cause of SHFLD. A similar to 11.8 kb minimal critical region was identified encompassing a single gene, BHLHA9, a putative basic loop helix transcription factor. Whole mount in situ hybridisation showed expression restricted to the limb bud mesenchyme underlying the apical ectodermal ridge in mouse and zebrafish embryos. Knock down of bhlha9 in zebrafish resulted in shortening of the pectoral fins. Conclusions Genomic duplications encompassing BHLHA9 are associated with SHFLD and non-Mendelian inheritance characterised by a high degree of non-penetrance with sex bias. Knock-down of bhlha9 in zebrafish causes severe reduction defects of the pectoral fin, indicating a role for this gene in limb development.

Increased frequency of the autism broader phenotype in mothers transmitting etiological CNVs to sons affected by Autism Spectrum Disorder (ASD)

Introduction: Autism Spectrum Disorder (ASD) is a frequent and complex neurodevelopmental disorder, characterized by impairments in social communication and repetitive behaviors and with a high male to female ratio: ~4:1. Genetic factors, including rare Copy Number Variants (CNVs), have a substantial impact in ASD risk 1, and are associated with specific phenotypic manifestations 2. Recent studies reported that rare inherited CNVs are enriched in mothers of ASD children compared with mothers of controls and are preferentially transmitted from mothers to ASD children suggesting a sex bias in CNV transmission; further, the imbalanced transmission of small pathogenic CNVs from unaffected mothers to their sons with ASD has been described 3, 4. An increased prevalence of autism - like personality traits is found in unaffected relatives of ASD children, suggesting a genetic liability of a broader autism phenotype (BAP) 5. The BAP in parents of autistic children can be assessed by the Social Responsiveness Scale (SRS) 6 and Broad Autism Phenotype Questionnaire (BAPQ) 7 reports . The SRS is 65 - item questionnaire to identify sub - clinical social impairments and interpersonal behaviour in individuals . The BAPQ is a 36 - item questionnaire measures social aloofness, rigid personality, and pragmatic language deficits in both parents and children.

Fine-scale spatial genetic correlation analyses reveal strong female philopatry within a brush-tailed rock-wallaby colony in southeast Queensland

We combine spatial data on home ranges of individuals and microsatellite markers to examine patterns of fine-scale spatial genetic structure and dispersal within a brush-tailed rock-wallaby (Petrogale penicillata) colony at Hurdle Creek Valley, Queensland. Brush-tailed rock-wallabies were once abundant and widespread throughout the rocky terrain of southeastern Australia; however, populations are nearly extinct in the south of their range and in decline elsewhere. We use pairwise relatedness measures and a recent multilocus spatial autocorrelation analysis to test the hypotheses that in this species, within-colony dispersal is male-biased and that female philopatry results in spatial clusters of related females within the colony. We provide clear evidence for strong female philopatry and male-biased dispersal within this rock-wallaby colony. There was a strong, significant negative correlation between pairwise relatedness and geographical distance of individual females along only 800 m of cliff line. Spatial genetic autocorrelation analyses showed significant positive correlation for females in close proximity to each other and revealed a genetic neighbourhood size of only 600 m for females. Our study is the first to report on the fine-scale spatial genetic structure within a rock-wallaby colony and we provide the first robust evidence for strong female philopatry and spatial clustering of related females within this taxon. We discuss the ecological and conservation implications of our findings for rock-wallabies, as well as the importance of fine-scale spatial genetic patterns in studies of dispersal behaviour.

Decreased relatedness between male prickly forest skinks (Gnypetoscincus queenslandiae) in habitat fragments

In species with low levels of dispersal the chance of closely related individuals breeding may be a potential problem; sex-biased dispersal is a mechanism that may decrease the possibility of cosanguineous mating. Fragmentation of the habitat in which a species lives may affect mechanisms such as sex-biased dispersal, which may in turn exacerbate more direct effects of fragmentation such as decreasing population size that may lead to inbreeding depression. Relatedness statistics calculated using microsatellite DNA data showed that rainforest fragmentation has had an effect on the patterns of dispersal in the prickly forest skink (Gnypetoscincus queenslandiae), a rainforest endemic of the Wet Tropics of north eastern Australia. A lower level of relatedness was found in fragments compared to continuous forest sites due to a significantly lower level of pairwise relatedness between males in rainforest fragments. The pattern of genetic relatedness between sexes indicates the presence of male-biased dispersal in this species, with a stronger pattern detected in populations in rainforest fragments. Male prickly forest skinks may have to move further in fragmented habitat in order to find mates or suitable habitat logs.

Increased frequency of the autism broader phenotype in mothers transmitting etiological CNVs to sons affected by Autism Spectrum Disorder (ASD)

Autism Spectrum Disorder (ASD) is a frequent and complex neurodevelopmental disorder, characterized by impairments in social communication and repetitive behaviors and with a high male to female ratio: ~4:1. Genetic factors, including rare Copy Number Variants (CNVs), have a substantial impact in ASD risk1, and are associated with specific phenotypic manifestations2. Recent studies reported that rare inherited CNVs are enriched in mothers of ASD children compared with mothers of controls and are preferentially transmitted from mothers to ASD children suggesting a sex bias in CNV transmission; further, the imbalanced transmission of small pathogenic CNVs from unaffected mothers to their sons with ASD has been described3,4. An increased prevalence of autism-like personality traits is found in unaffected relatives of ASD children, suggesting a genetic liability of a broader autism phenotype (BAP)5. The BAP in parents of autistic children can be assessed by the Social Responsiveness Scale (SRS)6 and Broad Autism Phenotype Questionnaire (BAPQ)7 reports. The SRS is 65-item questionnaire to identify sub-clinical social impairments and interpersonal behaviour in individuals. The BAPQ is a 36-item questionnaire measures social aloofness, rigid personality, and pragmatic language deficits in both parents and children.

Electro-cortical implicit race bias does not vary with participants' race or sex

Earlier research found evidence for electro-cortical race bias towards black target faces in white American participants irrespective of the task relevance of race. The present study investigated whether an implicit race bias generalizes across cultural contexts and racial in- and out-groups. An Australian sample of 56 Chinese and Caucasian males and females completed four oddball tasks that required sex judgements for pictures of male and female Chinese and Caucasian posers. The nature of the background (across task) and of the deviant stimuli (within task) was fully counterbalanced. Event-related potentials (ERPs) to deviant stimuli recorded from three midline sites were quantified in terms of mean amplitude for four components: N1, P2, N2 and a late positive complex (LPC; 350–700 ms). Deviants that differed from the backgrounds in sex or race elicited enhanced LPC activity. These differences were not modulated by participant race or sex. The current results replicate earlier reports of effects of poser race relative to background race on the LPC component of the ERP waveform. In addition, they indicate that an implicit race bias occurs regardless of participant's or poser's race and is not confined to a particular cultural context.

No evidence of bias from fish behavior in the selectivity of size and sex of the protogynous red porgy (Pagrus pagrus, Sparidae) by hook-and-line gear

Most fisheries select the size of fish to be caught (are size selective), and many factors, including gear, market demands, species distributions, fishery laws, and the behavior of both fishermen and fish, can contribute to that selectivity. Most fishing gear is size-selective and some, such as gill nets, are more so than others. The targeting behavior of fishermen is another key reason commercial and recreational fisheries tend to be size-selective. The more successful fishermen constantly seek areas and methods that yield larger or more profitable sizes of fish. Fishery regulations, especially size limits, produce size-selective harvests. Another factor with the potential to cause selectivity in a hook-and-line fishery is the different behavioral responses of fish to the bait or lure, whether the different responses arise among different fish sizes or between the sexes.

Sex allocation and local mate competition in Old World non-pollinating fig wasps

The populations of many species are structured such that mating is not random and occurs between members of local patches. When patches are founded by a single female and all matings occur between siblings, brothers may compete with each other for matings with their sisters. This local mate competition (LMC) selects for a female-biased sex ratio, especially in species where females have control over offspring sex, as in the parasitic Hymenoptera. Two factors are predicted to decrease the degree of female bias: (1) an increase in the number of foundress females in the patch and (2) an increase in the fraction of individuals mating after dispersal from the natal patch. Pollinating fig wasps are well known as classic examples of species where all matings occur in the local patch. We studied non-pollinating fig wasps, which are more diverse than the pollinating fig wasps and also provide natural experimental groups of species with different male morphologies that are linked to different mating structures. In this group of wasps, species with wingless males mate in the local patch (i.e. the fig fruit) while winged male species mate after dispersal. Species with both kinds of male have a mixture of local and non-local mating. Data from 44 species show that sex ratios (defined as the proportion of males) are in accordance with theoretical predictions: wingless male species < wing-dimorphic male species < winged male species. These results are also supported by a formal comparative analysis that controls for phylogeny. The foundress number is difficult to estimate directly for non-pollinating fig wasps but a robust indirect method leads to the prediction that foundress number, and hence sex ratio, should increase with the proportion of patches occupied in a crop. This result is supported strongly across 19 species with wingless males, but not across 8 species with winged males. The mean sex ratios for species with winged males are not significantly different from 0.5, and the absence of the correlation observed across species with wingless males may reflect weak selection to adjust the sex ratio in species whose population mating structure tends not to be subdivided. The same relationship is also predicted to occur within species if individual females adjust their sex ratios facultatively. This final prediction was not supported by data from a wingless male species, a male wing-dimorphic species or a winged male species.