Maternal genetic effects set the potential for evolution in a free-living vertebrate population

Heritable maternal effects have important consequences for the evolutionary dynamics of phenotypic traits under selection, but have only rarely been tested for or quantified in evolutionary studies. Here we estimate maternal effects on early-life traits in a feral population of Soay sheep (Ovis aries) from St Kilda, Scotland. We then partition the maternal effects into genetic and environmental components to obtain the first direct estimates of maternal genetic effects in a free-living population, and furthermore test for covariance between direct and maternal genetic effects. Using an animal model approach, direct heritabilities (h2) were low but maternal genetic effects (m2) represented a relatively large proportion of the total phenotypic variance for each trait (birth weight m2=0.119, birth date m2=0.197, natal litter size m2=0.211). A negative correlation between direct and maternal genetic effects was estimated for each trait, but was only statistically significant for natal litter size (ram= -0.714). Total heritabilities (incorporating variance from heritable maternal effects and the direct-maternal genetic covariance) were significant for birth weight and birth date but not for natal litter size. Inadequately specified models greatly overestimated additive genetic variance and hence direct h2 (by a factor of up to 6.45 in the case of birth date). We conclude that failure to model heritable maternal variance can result in over- or under-estimation of the potential for traits to respond to selection, and advocate an increased effort to explicitly measure maternal genetic effects in evolutionary studies.     

Molecular evolution of the vertebrate immune system

Adaptive immunity is unique to the vertebrates, and the molecules involved (including immunoglobulins, T cell receptors and the major histocompatibility complex molecules) seem to have diversified very rapidly early in vertebrate history. Reconstruction of gene phylogenies has yielded insights into the evolutionary origin of a number of molecular systems, including the complement system and the major histocompatibility complex (MHC). These analyses have indicated that the C5 component of complement arose by gene duplication prior to the divergence of C3 and C4, which suggests that the alternative complement pathway was the first to evolve. In the case of the MHC, phylogenetic analysis supports the hypothesis that MHC class II molecules evolved before class I molecules. The fact that the MHC-linked proteasome components that specifically produce peptides for presentation by class I MHC appear to have originated before the separation of jawed and jawless vertebrates suggests that the MHC itself may have been present at this time. Immmune system gene families have evolved by gene duplication, interlocus recombination and (in some cases) positive Darwinian selection favoring diversity at the amino acid level.     

Piecing together evolution of the vertebrate endocrine system

One of the great challenges in biology is to understand how particular complex morphological and physiological characters originated in specific evolutionary lineages. In this article, we address the origin of the vertebrate hypothalamic-pituitary-peripheral gland (H-P-PG) endocrine system, a complex network of specialized tissues, ligands and receptors. Analysis of metazoan nucleotide and protein sequences reveals a patchwork pattern of H-P-PG gene conservation between vertebrates and closely related invertebrates (ascidians). This is consistent with a model of how the vertebrate H-P-PG endocrine system could have emerged in relatively few steps by gene family expansion and by regulatory and structural modifications to genes that are present in a chordate ancestor. Some of these changes might have resulted in new connections between metabolic or signaling pathways, such as the bridging of 'synthesis islands' to form an efficient system for steroid hormone synthesis.     

Interacting gene clusters and the evolution of the vertebrate immune system

Unraveling the "code" of genome structure is an important goal of genomics research. Colocalization of genes in eukaryotic genomes may facilitate preservation of favorable allele combinations between epistasic loci or coregulation of functionally related genes. However, the presence of interacting gene clusters in the human genome has remained unclear. We systematically searched the human genome for evidence of closely linked genes whose protein products interact. We find 83 pairs of interacting genes that are located within 1 Mbp in the human genome or 37 if we exclude hub proteins. This number of interacting gene clusters is significantly more than expected by chance and is not the result of tandem duplications. Furthermore, we find that these clusters are significantly more conserved across vertebrate (but not chordate) genomes than other pairs of genes located within 1 Mbp in the human genome. In many cases, the genes are both present but not clustered in older vertebrate lineages. These results suggest gene cluster creation along the human lineage. These clusters are not enriched for housekeeping genes, but we find a significant contribution from genes involved in "response to stimulus." Many of these genes are involved in the immune response, including, but not limited to, known clusters such as the major histocompatibility complex. That these clusters were formed contemporaneously with the origin of adaptive immunity within the vertebrate lineage suggests that novel evolutionary and regulatory constraints were associated with the operation of the immune system.     

Indirect genetic effects and the genetic bases of social dominance: evidence from cattle

Genetic studies of social behaviour have currently received new impetus from models including indirect genetic effects (IGEs) of social partners. This study aimed at investigating the contribution of conspecifics in social dominance, considered as response of dyadic interaction that is, winning (dominant individual) or losing (subordinate). A genetic correlation of −1 is expected between the attitude to win and the attitude to loose, and because a population always accounts for half winners and half losers, the heritability of the dominant status should be close to zero. Specifically, social dominance was studied in Aosta Chestnut and Aosta Black Pied (Bos taurus) breeds, alpine rustic cattle famous for traditional tournaments where pairs of cows assess dominant status in bloodless fights. The outcomes of 25 590 dyadic interactions performed by 8159 individuals in 11 years were analysed by applying a classical quantitative model and models including indirect effects. Data were analysed via Bayesian approach on a threshold trait. The assessment of variances revealed a genetic correlation of −0.976 between direct and indirect genetic components. The heritability measured on a liability scale was 0.122 for direct phenotype, but decreased to 0.014 when the total heritable variance (TBV) was considered. The trend of estimated breeding values showed that the total TBV was constant over the years, even though its direct component increased and the indirect part decreased. This result confirms the relevance of IGEs on social behaviour and the assumption that the mean individual social dominance cannot evolve within a population, due to the evolutionary constraints imposed by the ‘social environment''.     

Indirect genetic effects from ecological interactions in Arabidopsis thaliana

Indirect genetic effects arise when genes expressed in one individual affect the expression of traits in other individuals. The importance of indirect genetic effects has been recognized for a diversity of evolutionary processes including kin selection, sexual selection, community structure and multilevel selection, but data regarding their genetic architecture and prevalence throughout the genome remain scarce, especially for interactions between unrelated individuals. Using a set of 411 Bay-0 x Shahdara Arabidopsis recombinant inbred lines grown with Landsberg neighbours, we examined quantitative trait loci (QTL) having direct and indirect effects on size, developmental, and fitness related traits. Using an interval mapping approach, we identified 15 QTL with direct effects and found that 13 of these QTL had significant indirect effects on trait expression in neighbouring plants. These results suggest widespread pleiotropy, as nearly all direct effect QTL have associated pleiotropic indirect effects. Paradoxically, most indirect effects were of the same sign as direct effects, creating a pattern of nearly universal positive pleiotropy that makes most covariances between direct and indirect effects positive. These results are consistent with a complex genetic basis for intraspecific interactions, but suggest that interactions between neighbouring plants are largely positive, rather than negative as would be expected for competition. In addition to their evolutionary and ecological importance, these pleiotropic relationships between DGE and IGE loci have implications for quantitative genetic studies of natural populations as well as experimental design considerations. Additionally, studies that ignore IGEs may over- or underestimate quantitative genetic parameters, as well as the effect of and variance contributed by QTL.     

Origin and evolution of the vertebrate vomeronasal system viewed through system-specific genes

Tetrapods have two distinct nasal chemosensory systems, the main olfactory system and the vomeronasal system (VNS). Defined by certain morphological components, the main olfactory system is present in all groups of vertebrates, while the VNS is found only in tetrapods. Previous attempts to identify a VNS precursor in teleost fish were limited by functional and morphological characters that could not clearly distinguish between homologous and analogous systems. In the past decade, several genes that specifically function in the VNS have been discovered. Here we first describe recent evolutionary studies of mammalian VNS-specific genes. We then review evidence showing the presence and tissue-specific expression of the VNS-specific genes in teleosts, as well as co-expression patterns of these genes in specific regions of the teleost olfactory epithelium. We propose that a VNS precursor exists in teleosts and that its evolutionary origin predated the separation between teleosts and tetrapods.     

Corticalization of two divisions of the visual system during vertebrate evolution

Data on the evolution of the visual system in vertebrate phylogeny are described. Visual projections are demonstrated in the telencephalon of cyclostomata (lampreys). The existence of a retino-thalamo-telencephalic pathway is demonstrated in elasmobranchs (skates). Two visual pathways are present in amphibians (frogs) and reptiles (turtles): retino-thalamo-telencephalic and retino-tecto-thalamo-telencephalic, and these overlap partly at the thalamic level in the lateral geniculate nucleus and completely in the telencephalon. In turtles the earliest visual and tectal impulses relay on their way to the telencephalon in the lateral geniculate body, and later impulses relay in the nucleus rotundus. In mammals (rats) visual tecto-cortical connections are seen; judging from the latent period of potentials arising in the visual cortex in response to stimulation of the superior colliculi these connections have one synaptic relay in the thalamus. The much shorter latent periods of visual evoked potentials recorded in the tectum of the monkey than in turtles (under identical chronic experimental conditions) confirm the views of morphologists on the progressive development of the tectal division of the visual system in vertebrate phylogeny. It is concluded that corticalization of both divisions of the visual system, i.e., the existence of telencephalic representation, appears in the early stages of vertebrate evolution.     

Heritabilities,social environment effects and genetic correlations of social behaviours in a cooperatively breeding vertebrate

Social animals interact frequently with conspecifics, and their behaviour is influenced by social context, environmental cues and the behaviours of interaction partners, allowing for adaptive, flexible adjustments to social encounters. This flexibility can be limited by part of the behavioural variation being genetically determined. Furthermore, behaviours can be genetically correlated, potentially constraining independent evolution. Understanding social behaviour thus requires carefully disentangling genetic, environmental, maternal and social sources of variations as well as the correlation structure between behaviours. Here, we assessed heritability, maternal, common environment and social effects of eight social behaviours in Neolamprologus pulcher, a cooperatively breeding cichlid. We bred wild‐caught fish in a paternal half‐sibling design and scored ability to defend a resource against conspecifics, to integrate into a group and the propensity to help defending the group territory (“helping behaviour”). We assessed genetic, social and phenotypic correlations within clusters of behaviours predicted to be functionally related, namely “competition,” “aggression,” “aggression‐sociability,” “integration” and “integration‐help.” Helping behaviour and two affiliative behaviours were heritable, whereas there was little evidence for a genetic basis in all other traits. Phenotypic social effects explained part of the variation in a sociable and a submissive behaviour, but there were no maternal or common environment effects. Genetic and phenotypic correlation within clusters was mostly positive. A group's social environment influenced covariances of social behaviours. Genetic correlations were similar in magnitude but usually exceeding the phenotypic ones, indicating that conclusions about the evolution of social behaviours in this species could be provisionally drawn from phenotypic data in cases where data for genetic analyses are unobtainable.     

Pathogen-induced rapid evolution in a vertebrate life-history trait

Anthropogenic factors, including climate warming, are increasing the incidence and prevalence of infectious diseases worldwide. Infectious diseases caused by pathogenic parasites can have severe impacts on host survival, thereby altering the selection regime and inducing evolutionary responses in their hosts. Knowledge about such evolutionary consequences in natural populations is critical to mitigate potential ecological and economic effects. However, studies on pathogen-induced trait changes are scarce and the pace of evolutionary change is largely unknown, particularly in vertebrates. Here, we use a time series from long-term monitoring of perch to estimate temporal trends in the maturation schedule before and after a severe pathogen outbreak. We show that the disease induced a phenotypic change from a previously increasing to a decreasing size at maturation, the most important life-history transition in animals. Evolutionary rates imposed by the pathogen were high and comparable to those reported for populations exposed to intense human harvesting. Pathogens thus represent highly potent drivers of adaptive phenotypic evolution in vertebrates.     

The effects of genetic drift in experimental evolution

Experimental evolution is characterized by exponential or logistic growth and periodic population bottlenecks. The fate of a rare beneficial mutation in these systems is influenced both by the bottleneck effect and by genetic drift. This paper explores the effects of incorporating genetic drift into models of fixation probability in populations with periodic bottlenecks. To model the inherent stochasticity during the growth phase in these populations, we assume a Poisson distribution of offspring. An analytical solution is developed to calculate the fixation probability and a computer simulation is used to verify the results. We find that the fixation rate of a favourable mutant is significantly lower when genetic drift is considered; fixation probability is reduced by over 25% for realistic experimental protocols. Our method is valid for both weak and strong selection; since very large selection coefficients have been reported in the experimental literature, this is an important improvement over previous results.     

Indirect plant-mediated effects on insect immunity and disease resistance in a tritrophic system

Host plant quality can significantly influence the growth and condition of phytophagous insects, and consequently their susceptibility to pathogens. This study examined the relationship between host plant quality, insect condition, immune responsiveness and resistance to pathogens in the cabbage looper, Trichoplusia ni. Two baseline and induced immune parameters were estimated, haemocyte numbers and haemolymph phenoloxidase (PO) activity, for larvae on two host plants, broccoli and cucumber. Haemolymph protein concentration was assessed as an indication of insect condition, and the susceptibility of larvae to T. ni single nucleopolyhedrovirus (SNPV) was used as a measure of disease resistance. T. ni growth, survival and condition was much higher on broccoli than cucumber. Haemocyte numbers were significantly higher in broccoli-reared larvae, whereas PO activity was not. An immune challenge induced significantly elevated numbers of haemocytes for larvae reared on both host plants, but did not affect PO activity or protein concentrations. Susceptibility to T. ni SNPV was markedly higher in larvae reared on cucumber than on broccoli. These results clearly indicate that host plant quality can affect both immune response and disease resistance of T. ni larvae and that bottom-up effects could be important in interactions between insects and entomopathogens.