Jessica Stapley

The genome of a songbird.

The zebra finch is an important model organism in several fields with unique relevance to human neuroscience. Like other songbirds, the zebra finch communicates through learned vocalizations, an ability otherwise documented only in humans and a few other animals and lacking in the chicken—the only bird with a sequenced genome until now. Here we present a structural, functional and comparative analysis of the genome sequence of the zebra finch (Taeniopygia guttata), which is a songbird belonging to the large avian order Passeriformes. We find that the overall structures of the genomes are similar in zebra finch and chicken, but they differ in many intrachromosomal rearrangements, lineage-specific gene family expansions, the number of long-terminal-repeat-based retrotransposons, and mechanisms of sex chromosome dosage compensation. We show that song behaviour engages gene regulatory networks in the zebra finch brain, altering the expression of long non-coding RNAs, microRNAs, transcription factors and their targets. We also show evidence for rapid molecular evolution in the songbird lineage of genes that are regulated during song experience. These results indicate an active involvement of the genome in neural processes underlying vocal communication and identify potential genetic substrates for the evolution and regulation of this behaviour.

Adaptation genomics: the next generation

Understanding the genetics of how organisms adapt to changing environments is a fundamental topic in modern evolutionary ecology. The field is currently progressing rapidly because of advances in genomics technologies, especially DNA sequencing. The aim of this review is to first briefly summarise how next generation sequencing (NGS) has transformed our ability to identify the genes underpinning adaptation. We then demonstrate how the application of these genomic tools to ecological model species means that we can start addressing some of the questions that have puzzled ecological geneticists for decades such as: How many genes are involved in adaptation? What types of genetic variation are responsible for adaptation? Does adaptation utilise pre-existing genetic variation or does it require new mutations to arise following an environmental change?

Gene mapping in the wild with SNPs: guidelines and future directions

One of the biggest challenges facing evolutionary biologists is to identify and understand loci that explain fitness variation in natural populations. This review describes how genetic (linkage) mapping with single nucleotide polymorphism (SNP) markers can lead to great progress in this area. Strategies for SNP discovery and SNP genotyping are described and an overview of how to model SNP genotype information in mapping studies is presented. Finally, the opportunity afforded by new generation sequencing and typing technologies to map fitness genes by genome-wide association studies is discussed.

Ecological example of conditioned flavor aversion in plant-herbivore interactions: Effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums

We investigated the hypothesis that feeding deterrence of common ringtail possums (Pseudocheirus peregrinus) and common brushtail possums (Trichosurus vulpecula) by Eucalyptus terpenes (in this case 1,8-cineole) is a result of a conditioned flavor aversion (CFA), due to the association of terpenes with postingestive effects of another group of Eucalyptus toxins, the diformylphloroglucinol compounds (DFPCs). Wild-caught common ringtail and common brushtail possums showed a dose-dependent reduction in food intake when 1,8-cineole was added to the diet. However, after continued exposure over 12 days to increasing amounts of cineole in the diet, both species substantially increased their intakes of cineole relative to control animals. This indicated that the aversion to cineole was a conditioned response rather than a physiological limitation in their ability to detoxify terpenes. Subsequent exposure to a diet including both cineole and jensenone (a simple DFPC also found in Eucalyptus and considered to cause postingestive emesis) in corresponding amounts was able to recondition the dose-dependent aversion. Consequently, animals that had been given jensenone showed an aversion to cineole-rich diets that matched the behavior of animals in the control group. This supported our hypothesis that the effect of terpenes on feeding of these marsupial folivores on Eucalyptus is due to a CFA. Possums can cope with levels of terpenes in the diet that far exceed those occurring naturally. The role of terpenes in marsupial folivore–Eucalyptus interactions appears to be to act as a cue to levels of toxic DFPCs in the leaves, rather than acting as toxins in their own right.

A Linkage Map of the Zebra Finch Taeniopygia guttata Provides New Insights Into Avian Genome Evolution

Passeriformes are the largest order of birds and one of the most widely studied groups in evolutionary biology and ecology. Until recently genomic tools in passerines relied on chicken genomic resources. Here we report the construction and analysis of a whole-genome linkage map for the zebra finch (Taeniopygia guttata) using a 354-bird pedigree. The map contains 876 SNPs dispersed across 45 linkage groups and we found only a few instances of interchromosomal rearrangement between the zebra finch and the chicken genomes. Interestingly, there was a greater than expected degree of intrachromosomal rearrangements compared to the chicken, suggesting that gene order is not conserved within avian chromosomes. At 1068 cM the map is approximately only one quarter the length of the chicken linkage map, providing further evidence that the chicken has an unusually high recombination rate. Male and female linkage-map lengths were similar, suggesting no heterochiasmy in the zebra finch. This whole-genome map is the first for any passerine and a valuable tool for the zebra finch genome sequence project and for studies of quantitative trait loci.

On the use of large marker panels to estimate inbreeding and relatedness: empirical and simulation studies of a pedigreed zebra finch population typed at 771 SNPs

In recent years there has been a dramatic increase in the availability of high density genetic marker data for both model and non‐model organisms. A potential application of these data is to infer relatedness in the absence of a complete pedigree. Using a marker panel of 771 SNPs genotyped in three generations of an extensive zebra finch pedigree, correlations between pedigree relatedness and seven marker‐based estimates of relatedness were examined, as was the relationship between heterozygosity and inbreeding. Although marker‐based and pedigree relatedness were highly correlated, the variance in estimated relatedness was high. Further, the correlation between heterozygosity and inbreeding was weak, even though mean inbreeding coefficient is typical of that seen in wild vertebrate pedigrees; the weak relationship was in part due to the small variance in inbreeding in the pedigree. Our data suggest that using marker information to reconstruct the pedigree, and then calculating relatedness from the pedigree, is likely to give more accurate relatedness estimates than using marker‐based estimators directly.

Ultraviolet signals fighting ability in a lizard

Ultraviolet (UV) signals are used in female mate choice in numerous taxa; however, the role of UV signals in male contests remains relatively unexplored. We experimentally reduced throat UV of free-ranging lizards (Platysaurus broadleyi) to test whether UV acts as a signal of fighting ability during male contests. We found that UV-reduced males were more likely to be challenged than control males. However, contest outcome was not influenced by UV-reduction, and this was despite other obvious asymmetries between opponents, such as body size and residency. Throat UV was confirmed as a signal of fighting ability because contests were more likely to escalate when one contestant had reduced UV. Therefore, throat UV, not body size or residency, was used during the initial stage of opponent assessment, but this did not influence contest outcome. The results suggest that UV overrides other traits that could function as signals during rival assessment.

A comparison of SNPs and microsatellites as linkage mapping markers: lessons from the zebra finch (Taeniopygia guttata)

BackgroundGenetic linkage maps are essential tools when searching for quantitative trait loci (QTL). To maximize genome coverage and provide an evenly spaced marker distribution a combination of different types of genetic marker are sometimes used. In this study we created linkage maps of four zebra finch (Taeniopygia guttata) chromosomes (1, 1A, 2 and 9) using two types of marker, Single Nucleotide Polymorphisms (SNPs) and microsatellites. To assess the effectiveness and accuracy of each kind of marker we compared maps built with each marker type separately and with both types of marker combined. Linkage map marker order was validated by making comparisons to the assembled zebra finch genome sequence.ResultsWe showed that marker order was less reliable and linkage map lengths were inflated for microsatellite maps relative to SNP maps, apparently due to differing error rates between the two types of marker. Guidelines on how to minimise the effects of error are provided. In particular, we show that when combining both types of marker the conventional process of building linkage maps, whereby the most informative markers are added to the map first, has to be modified in order to improve map accuracy.ConclusionsWhen using multiple types and large numbers of markers to create dense linkage maps, the least error prone loci (SNPs) rather than the most informative should be used to create framework maps before the addition of other potentially more error prone markers (microsatellites). This raises questions about the accuracy of marker order and predicted recombination rates in previous microsatellite linkage maps which were created using the conventional building process, however, provided suitable error detection strategies are followed microsatellite-based maps can continue to be regarded as reasonably reliable.

Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species

Rapid adaptation of invasive species to novel habitats has puzzled evolutionary biologists for decades, especially as this often occurs in the face of limited genetic variability. Although some ecological traits common to invasive species have been identified, little is known about the possible genomic/genetic mechanisms that may underlie their success. A common scenario in many introductions is that small founder population sizes will often lead to reduced genetic diversity, but that invading populations experience large environmental perturbations, such as changes in habitat and environmental stress. Although sudden and intense stress is usually considered in a negative context, these perturbations may actually facilitate rapid adaptation by affecting genome structure, organization and function via interactions with transposable elements (TEs), especially in populations with low genetic diversity. Stress‐induced changes in TE activity can alter gene action and can promote structural variation that may facilitate the rapid adaptation observed in new environments. We focus here on the adaptive potential of TEs in relation to invasive species and highlight their role as powerful mutational forces that can rapidly create genetic diversity. We hypothesize that activity of transposable elements can explain rapid adaptation despite low genetic variation (the genetic paradox of invasive species), and provide a framework under which this hypothesis can be tested using recently developed and emerging genomic technologies.

Exploratory and antipredator behaviours differ between territorial and nonterritorial male lizards

Alternative territorial tactics may be part of a broader behavioural tendency that can influence the expression of other behavioural traits. We compared the exploratory and predator avoidance behaviours of territorial and floater male water skinks, Eulamprus heatwolei, to identify whether these alternative behavioural tactics are part of a broader behavioural dichotomy. Floater and territorial males differed in their tendencies to explore novel habitats. Floaters spent less time in the refuge, moved further and ate more mealworms when placed in a novel enclosure, suggesting that floaters were less wary of the novel environment and had greater exploratory tendencies. Predator avoidance behaviours also differed between the two groups of males. Territorial lizards were less likely to retreat to a refuge site during a simulated predator attack, returned faster to a basking site after this attack and as a result had a smaller net reduction in preattack body temperature. These results may be attributed to the trade-off that territorial lizards face between territorial defence and antipredator behaviour, which floaters do not experience. Our results suggest that territorial tactics may be part of a broader behavioural tendency that can influence the expression and evolution of other seemingly unrelated traits.