Travis C. Collier

Genome complexity, robustness and genetic interactions in digital organisms

Digital organisms are computer programs that self-replicate, mutate and adapt by natural selection. They offer an opportunity to test generalizations about living systems that may extend beyond the organic life that biologists usually study. Here we have generated two classes of digital organism: simple programs selected solely for rapid replication, and complex programs selected to perform mathematical operations that accelerate replication through a set of defined ‘metabolic’ rewards. To examine the differences in their genetic architecture, we introduced millions of single and multiple mutations into each organism and measured the effects on the organisms fitness. The complex organisms are more robust than the simple ones with respect to the average effects of single mutations. Interactions among mutations are common and usually yield higher fitness than predicted from the component mutations assuming multiplicative effects; such interactions are especially important in the complex organisms. Frequent interactions among mutations have also been seen in bacteria, fungi and fruitflies. Our findings support the view that interactions are a general feature of genetic systems.

An empirical study of collaborative acoustic source localization

Field biologists use animal sounds to discover the presence of individuals and to study their behavior. Collecting bio- acoustic data has traditionally been a difficult and time- consuming process in which researchers use portable microphones to record sounds while taking notes of their own detailed observations. The recent development of new deploy- able acoustic sensor platforms presents opportunities to develop automated tools for bio-acoustic field research. In this work, we implement an AML-based source localization algorithm, and use it to localize marmot alarm-calls. We assess the performance of these techniques based on results from two field experiments: (1) a controlled test of direction-of- arrival (DOA) accuracy using a pre-recorded source signal, and (2) an experiment to detect and localize actual animals in their habitat, with a comparison to ground truth gathered from human observations. Although small arrays yield ambiguities from spatial aliasing of high frequency signals, we show that these ambiguities are readily eliminated by proper bearing crossings of the DOAs from several arrays. These results show that the AML source localization algorithm can be used to localize actual animals in their natural habitat, using a platform that is practical to deploy.

Adaptive introgression in an African malaria mosquito coincident with the increased usage of insecticide-treated bed nets

Significance We report that during a recent period of hybridization between two major African malaria mosquitoes, Anopheles gambiae and Anopheles coluzzii, an island of divergence on chromosome 2 introgressed from the A. gambiae into the A. coluzzii genome and its frequency subsequently increased. This introgression was coincident with the start of a major insecticide-treated bed net campaigns in Mali. These observations suggest that increased insecticide exposure acted as a selective force sufficient to drive introgression of an entire genomic island of divergence across the reproductive barrier separating these two species. This study provides a rare example of adaptive introgression in an animal species and elucidates the dynamics of how insecticide resistance evolved in A. coluzzii. Animal species adapt to changes in their environment, including man-made changes such as the introduction of insecticides, through selection for advantageous genes already present in populations or newly arisen through mutation. A possible alternative mechanism is the acquisition of adaptive genes from related species via a process known as adaptive introgression. Differing levels of insecticide resistance between two African malaria vectors, Anopheles coluzzii and Anopheles gambiae, have been attributed to assortative mating between the two species. In a previous study, we reported two bouts of hybridization observed in the town of Selinkenyi, Mali in 2002 and 2006. These hybridization events did not appear to be directly associated with insecticide-resistance genes. We demonstrate that during a brief breakdown in assortative mating in 2006, A. coluzzii inherited the entire A. gambiae-associated 2L divergence island, which includes a suite of insecticide-resistance alleles. In this case, introgression was coincident with the start of a major insecticide-treated bed net distribution campaign in Mali. This suggests that insecticide exposure altered the fitness landscape, favoring the survival of A. coluzzii/A. gambiae hybrids, and provided selection pressure that swept the 2L divergence island through A. coluzzii populations in Mali. We propose that the work described herein presents a unique description of the temporal dynamics of adaptive introgression in an animal species and represents a mechanism for the rapid evolution of insecticide resistance in this important vector of human malaria in Africa.

Self-organization in sensor networks

In an effort to better guide research into self-confguring wireless sensor networks, we discuss a technical defnition of the term self-organization. We define a self-organizing system as one where a collection of units coordinate with each other to form a system that adapts to achieve a goal more efficiently. We then lay out some conditions that must hold for a system to meet this definition and discuss some examples of self-organizing systems. Finally, we explore some of the ways this definition applies to wireless sensor networks.

Spatiotemporal dynamics of gene flow and hybrid fitness between the M and S forms of the malaria mosquito, Anopheles gambiae

Significance Populations of the African malaria vector, Anopheles gambiae, are structured into M and S forms. All current work assumes the two rarely hybridize. Here we show this assumption is false. We demonstrate (i) significant exchange of genes between the two forms, even though (ii) hybrids have reduced fitness and (iii) the gene exchange process is spatially and temporally dynamic. For malaria, it is important to determine if genes for traits like insecticide resistance are shared between forms. For evolutionary biologists, this work confirms that this mosquito is a good model for studying if and how species may evolve in cases where there is ongoing gene flow. The M and S forms of Anopheles gambiae have been the focus of intense study by malaria researchers and evolutionary biologists interested in ecological speciation. Divergence occurs at three discrete islands in genomes that are otherwise nearly identical. An “islands of speciation” model proposes that diverged regions contain genes that are maintained by selection in the face of gene flow. An alternative “incidental island” model maintains that gene flow between M and S is effectively zero and that divergence islands are unrelated to speciation. A “divergence island SNP” assay was used to explore the spatial and temporal distributions of hybrid genotypes. Results revealed that hybrid individuals occur at frequencies ranging between 5% and 97% in every population examined. A temporal analysis revealed that assortative mating is unstable and periodically breaks down, resulting in extensive hybridization. Results suggest that hybrids suffer a fitness disadvantage, but at least some hybrid genotypes are viable. Stable introgression of the 2L speciation island occurred at one site following a hybridization event.

Selective pressures on genomes in molecular evolution.

We describe the evolution of macromolecules as an information transmission process and apply tools from Shannon information theory to it. This allows us to isolate three independent, competing selective pressures that we term compression, transmission, and neutrality selection. The first two affect genome length: the pressure to conserve resources by compressing the code, and the pressure to acquire additional information that improves the channel, increasing the rate of information transmission into each offspring. Noisy transmission channels (replication with mutations) give rise to a third pressure that acts on the actual encoding of information; it maximizes the fraction of mutations that are neutral with respect to the phenotype. This neutrality selection has important implications for the evolution of evolvability. We demonstrate each selective pressure in experiments with digital organisms.

An Empirical Study of Collaborative Acoustic Source Localization

Field biologists use animal sounds to discover the presence of individuals and to study their behavior. Collecting bio-acoustic data has traditionally been a difficult and time-consuming process in which researchers use portable microphones to record sounds while taking notes of their own detailed observations. The recent development of new deployable acoustic sensor platforms presents opportunities to develop automated tools for bio-acoustic field research. In this work, we implement both two-dimensional (2D) and three-dimensional (3D) AML-based source localization algorithms. The 2D algorithm is used to localize marmot alarm-calls of marmots on the meadow ground. The 3D algorithm is used to localize the song of Acorn Woodpecker and Mexican Antthrush birds situated above the ground. We assess the performance of these techniques based on the results from four field experiments: two controlled test of direction-of-arrival (DOA) accuracy using a pre-recorded source signal for 2D and 3D analysis, an experiment to detect and localize actual animals in their habitat, with a comparison to ground truth gathered from human observations, and a controlled test of localization experiment using pre-recorded source to enable careful ground truth measurements. Although small arrays yield ambiguities from spatial aliasing of high frequency signals, we show that these ambiguities are readily eliminated by proper bearing crossings of the DOAs from several arrays. These results show that the AML source localization algorithm can be used to localize actual animals in their natural habitat using a platform that is practical to deploy.

Acoustic localization of antbirds in a Mexican rainforest using a wireless sensor network

Acoustic localization is a promising method to passively observe vocal animal species, but remains difficult and time consuming to employ. To reduce the labor intensity and impact of deployment, an acoustic localization system has been developed consisting of battery powered wireless sensor nodes. The system also has the ability to perform an acoustic self-survey, which compares favorably in accuracy to global positioning system survey methods, especially in environments such as forest. The self-survey and localization accuracy of the system was tested in the neotropical rainforest of Chiapas, Mexico. A straight-forward and robust correlation sum localization computation method was utilized and is described in detail. Both free-ranging wild antbird songs and songs played from a speaker were localized with mean errors of 0.199 m and 0.445 m, respectively. Finally, additional tests utilizing only a short segment of each song or a subset of sensor nodes were performed and found to minimally affect localization accuracy. The use of a wireless sensor network for acoustic localization of animal vocalizations offers greater ease and flexibility of deployment than wired microphone arrays without sacrificing accuracy.

Chromosome inversions, genomic differentiation and speciation in the African malaria mosquito Anopheles gambiae.

The African malaria vector, Anopheles gambiae, is characterized by multiple polymorphic chromosomal inversions and has become widely studied as a system for exploring models of speciation. Near complete reproductive isolation between different inversion types, known as chromosomal forms, has led to the suggestion that A. gambiae is in early stages of speciation, with divergence evolving in the face of considerable gene flow. We compared the standard chromosomal arrangement (Savanna form) with genomes homozygous for j, b, c, and u inversions (Bamako form) in order to identify regions of genomic divergence with respect to inversion polymorphism. We found levels of divergence between the two sub-taxa within some of these inversions (2Rj and 2Rb), but at a level lower than expected and confined near the inversion breakpoints, consistent with a gene flux model. Unexpectedly, we found that the majority of diverged regions were located on the X chromosome, which contained half of all significantly diverged regions, with much of this divergence located within exons. This is surprising given that the Bamako and Savanna chromosomal forms are both within the S molecular form that is defined by a locus near centromere of X chromosome. Two X-linked genes (a heat shock protein and P450 encoding genes) involved in reproductive isolation between the M and S molecular forms of A. gambiae were also significantly diverged between the two chromosomal forms. These results suggest that genes mediating reproductive isolation are likely located on the X chromosome, as is thought to be the case for the M and S molecular forms. We conclude that genes located on the sex chromosome may be the major force driving speciation between these chromosomal forms of A. gambiae.

The Genetic Basis of Host Preference and Resting Behavior in the Major African Malaria Vector, Anopheles arabiensis

Malaria transmission is dependent on the propensity of Anopheles mosquitoes to bite humans (anthropophily) instead of other dead end hosts. Recent increases in the usage of Long Lasting Insecticide Treated Nets (LLINs) in Africa have been associated with reductions in highly anthropophilic and endophilic vectors such as Anopheles gambiae s.s., leaving species with a broader host range, such as Anopheles arabiensis, as the most prominent remaining source of transmission in many settings. An. arabiensis appears to be more of a generalist in terms of its host choice and resting behavior, which may be due to phenotypic plasticity and/or segregating allelic variation. To investigate the genetic basis of host choice and resting behavior in An. arabiensis we sequenced the genomes of 23 human-fed and 25 cattle-fed mosquitoes collected both in-doors and out-doors in the Kilombero Valley, Tanzania. We identified a total of 4,820,851 SNPs, which were used to conduct the first genome-wide estimates of “SNP heritability” for host choice and resting behavior in this species. A genetic component was detected for host choice (human vs cow fed; permuted P = 0.002), but there was no evidence of a genetic component for resting behavior (indoors versus outside; permuted P = 0.465). A principal component analysis (PCA) segregated individuals based on genomic variation into three groups which were characterized by differences at the 2Rb and/or 3Ra paracentromeric chromosome inversions. There was a non-random distribution of cattle-fed mosquitoes between the PCA clusters, suggesting that alleles linked to the 2Rb and/or 3Ra inversions may influence host choice. Using a novel inversion genotyping assay, we detected a significant enrichment of the standard arrangement (non-inverted) of 3Ra among cattle-fed mosquitoes (N = 129) versus all non-cattle-fed individuals (N = 234; χ2, p = 0.007). Thus, tracking the frequency of the 3Ra in An. arabiensis populations may be of use to infer selection on host choice behavior within these vector populations; possibly in response to vector control. Controlled host-choice assays are needed to discern whether the observed genetic component has a direct relationship with innate host preference. A better understanding of the genetic basis for host feeding behavior in An. arabiensis may also open avenues for novel vector control strategies based on driving genes for zoophily into wild mosquito populations.