Linear Control Theory for Gene Network Modeling

Systems biology is an interdisciplinary field that aims at understanding complex interactions in cells. Here we demonstrate that linear control theory can provide valuable insight and practical tools for the characterization of complex biological networks. We provide the foundation for such analyses through the study of several case studies including cascade and parallel forms, feedback and feedforward loops. We reproduce experimental results and provide rational analysis of the observed behavior. We demonstrate that methods such as the transfer function (frequency domain) and linear state-space (time domain) can be used to predict reliably the properties and transient behavior of complex network topologies and point to specific design strategies for synthetic networks.     

Heuristics or general learning processes?

The concept of heuristics implies that the rules governing choice behavior may vary with ecological constraints. Behavior analysis, in contrast, seeks general principles that transcend specific situations. To the extent that search is successful, the concept of heuristics is unlikely to play a significant role in the analysis of animal behavior.     

Uncertainty causes humans to use social heuristics and to cooperate more: An experiment among Belgian university students

When humans engage in social interactions, they are often uncertain about what the possible outcomes are. Because of this, highly sophisticated cooperation strategies may not be very effective. Indeed, some models instead predict the emergence of ‘social heuristics’: simple cooperation strategies that perform well across a range of different situations. Here, we put these predictions to the test in a large-scale interactive decision making experiment. We confronted participants (mostly Belgian university students) with a broad range of cooperative interactions, systematically varying the uncertainty participants had about the consequences of cooperating. As expected, we find that uncertainty about the payoff consequences of cooperation causes individuals to use social heuristics. Additionally, these heuristics directly cause a marked increase in cooperation compared to the treatment without uncertainty, even in situations where cooperation can never be beneficial. These findings provide a new explanation for why human social behavior often violates the standard predictions of economic and evolutionary theory.     

Population genetics strategies to characterize long-distance dispersal of insects

Population genetics strategies offer an alternative and powerful approach for obtaining information about long-distance movement, and have been widely used for examining patterns and magnitude of insect dispersal over geographic and temporal scales. Such strategies are based on the principle that genetic divergence between local populations reflects the interplay between genetic drift and gene flow, and thus can function as an indicator of dispersal capacity. Relatively new approaches for inferring population history are widely applicable for documenting introduction routes of invasive or quarantine species. These approaches are based on genetic variability calculated from changes in gene frequency of subpopulations, measured using molecular genetic markers. Inferences from population genetics can supplement and corroborate conventional observational approaches for characterizing insect dispersal and have provided important clues to many questions raised in the field of behavior and ecology of insects. Here, we summarize our work on the boll weevil as a case study to illustrate the kinds of information on dispersal capacity and dispersal patterns that can be obtained from population genetics techniques that would be difficult or impossible to acquire in other ways. Then we provide examples of how the molecular markers and population genetics tools have been applied to answer immediate questions of relevance to eradication program managers. Though the latter are idiosyncratic to this particular pest, they demonstrate the kinds and range of problems that can be addressed in other systems through application of population genetics strategies.     

Sociobiology and the Comparative Approach: One Way to Study Ourselves

This paper is based on my lecture in a macroevolution course I team-teach with Profs. Daniel Brooks and David Evans at the University of Toronto. The lecture has undergone many revisions over the years as I grappled with problems discussing certain areas (e.g., rape as an adaptive strategy, gender “roles”). Eventually, I realized that the problem areas said more about my personal conflicts than they did about the science. This was one of those epiphany moments, a time when I recognized that I was less likely to accept hypotheses that contradicted the way I wanted the world to be and more likely to uncritically accept hypotheses that confirmed my world view. That epiphany, in turn, led me to realize that science is never separate from the personal biases/demons of its practitioners, especially when we are asking questions about the evolution of human behavior. That realization was not novel within the vast literature of sociology and philosophy. But it was novel for me. I was aware of discussions about personal biases clouding scientific interpretation; I just didn’t think it applied to me (I absorbed the philosophical discussions without making the connection to “my world”). So, on the heels of that epiphany, the following is a very personal take on the question of teaching sociobiology, based on where my journey, aided by my experience as an ethologist and phylogeneticist and colored by my own history, has taken me.     

Alloparental behavior in a captive group of spider monkeys (Ateles geoffroyi) at the Auckland zoo

I studied alloparental behavior in a captive group of spider monkeys at the Auckland Zoo using seven infants as focal subjects and assessed the effects of age, sex, and reproductive status of alloparents on patterns of infant-other interaction. Adult males initiated interactions with infants most often, followed by adult females. Immature individuals interacted with infants infrequently. Infants themselves initiated contact with adult males more often than with other members of the group. Alloparental behavior in spider monkeys differs from that in most other species in that the infant is an active rather than a passive participant in alloparental interactions. I discuss the patterns of infant-other interaction in relation to the social structure and dispersal patterns of Ateles.     

New approaches to phylogenetic tree search and their application to large numbers of protein alignments

Phylogenetic tree estimation plays a critical role in a wide variety of molecular studies, including molecular systematics, phylogenetics, and comparative genomics. Finding the optimal tree relating a set of sequences using score-based (optimality criterion) methods, such as maximum likelihood and maximum parsimony, may require all possible trees to be considered, which is not feasible even for modest numbers of sequences. In practice, trees are estimated using heuristics that represent a trade-off between topological accuracy and speed. I present a series of novel algorithms suitable for score-based phylogenetic tree reconstruction that demonstrably improve the accuracy of tree estimates while maintaining high computational speeds. The heuristics function by allowing the efficient exploration of large numbers of trees through novel hill-climbing and resampling strategies. These heuristics, and other computational approximations, are implemented for maximum likelihood estimation of trees in the program Leaphy, and its performance is compared to other popular phylogenetic programs. Trees are estimated from 4059 different protein alignments using a selection of phylogenetic programs and the likelihoods of the tree estimates are compared. Trees estimated using Leaphy are found to have equal to or better likelihoods than trees estimated using other phylogenetic programs in 4004 (98.6%) families and provide a unique best tree that no other program found in 1102 (27.1%) families. The improvement is particularly marked for larger families (80 to 100 sequences), where Leaphy finds a unique best tree in 81.7% of families.     

Return of the Native: Cognition and Site-Specific Expertise in Orangutan Rehabilitation

Ex-captive orangutans that have returned to free forest life in Bornean forests offer exceptional opportunities to assess the cognitive challenges facing feral great apes. They also provide opportunities to track readaptation, which requires building expertise to survive in tropical rain forests and to integrate into orangutan communities. I outline some of the foraging problems that ex-captive orangutans encounter, the cognitive processes used in their solutions, and acquisition patterns. Evidence derives primarily from observational studies of feeding behavior in free-ranging ex-captives. Discussion focuses on implications for conservation initiatives.     

Sequence-based heuristics for faster annotation of non-coding RNA families

MOTIVATION: Non-coding RNAs (ncRNAs) are functional RNA molecules that do not code for proteins. Covariance Models (CMs) are a useful statistical tool to find new members of an ncRNA gene family in a large genome database, using both sequence and, importantly, RNA secondary structure information. Unfortunately, CM searches are extremely slow. Previously, we created rigorous filters, which provably sacrifice none of a CM's accuracy, while making searches significantly faster for virtually all ncRNA families. However, these rigorous filters make searches slower than heuristics could be. RESULTS: In this paper we introduce profile HMM-based heuristic filters. We show that their accuracy is usually superior to heuristics based on BLAST. Moreover, we compared our heuristics with those used in tRNAscan-SE, whose heuristics incorporate a significant amount of work specific to tRNAs, where our heuristics are generic to any ncRNA. Performance was roughly comparable, so we expect that our heuristics provide a high-quality solution that--unlike family-specific solutions--can scale to hundreds of ncRNA families. AVAILABILITY: The source code is available under GNU Public License at the supplementary web site.     

Distribution of myogenic progenitor cells and myonuclei is altered in women with vs. those without chronically painful trapezius muscle

It is hypothesized that repeated recruitment of low-threshold motor units is an underlying cause of chronic pain in trapezius myalgia. This study investigated the distribution of satellite cells (SCs), myonuclei, and macrophages in muscle biopsies from the trapezius muscle of 42 women performing repetitive manual work, diagnosed with trapezius myalgia (MYA; 44 ± 8 yr; mean ± SD) and 20 matched healthy controls (CON; 45 ± 9 yr). Our hypothesis was that muscle of MYA, in particular type I fibers, would demonstrate higher numbers of SCs, myonuclei, and macrophages compared with CON. SCs were identified on muscle cross sections by combined immunohistochemical staining for Pax7, type I myosin, and laminin, allowing the number of SCs associated with type I and II fibers to be determined. We observed a pattern of SC distribution in MYA previously only reported for individuals above 70 yr of age. Compared with CON, MYA demonstrated 19% more SCs per fiber associated with type I fibers (MYA 0.098 ± 0.039 vs. CON 0.079 ± 0.031; P < 0.05) and 40% fewer SCs associated with type II fibers (MYA 0.047 ± 0.017 vs. CON 0.066 ± 0.035; P < 0.05). The finding of similar numbers of macrophages between the two groups was not in line with our hypothesis and suggests that the elevated SC content of MYA was not due to heightened inflammatory cell contents, but rather to provide new myonuclei. The findings of greater numbers of SCs in type I fibers of muscle subjected to repeated low-intensity work support our hypothesis and provide new insight into stimuli capable of regulating SC content.     

Avoiding Predators: Expectations and Evidence in Primate Antipredator Behavior

Predation and antipredator behavior are important but poorly studied influences on the evolution of primate societies. I review recent evidence of predation and antipredator strategies among primates. I describe patterns of antipredator behavior and attempt to explain the variation among primate taxa and among antipredator strategies. I use predation by chimpanzees on red colobus and antipredator strategies by the colobus as a case study of how a primate prey species may respond to the threat of predation.     

Foraging ecomorphology within North American flycatchers and a test of concordance with southern African species

In both the Old and New Worlds, independent clades of sit-and-wait insectivorous birds have evolved. These independent radiations provide an excellent opportunity to test whether the relationships between morphology and ecology are concordant among different communities of flycatchers. First, with canonical correlation analysis, I test for significant relationships between foraging behavior and morphology in North American (NA) and southern African (SA) flycatcher communities. Second, using ordination and analysis of covariance, I test for concordant ecomorphological relationships between the localities. Also, I accounted for phylogeny to see if observed patterns were adaptive. Morphology predicted the foraging behavior in both NA and SA flycatchers. Smaller bill features and longer legs are related to perching and attacking prey items near or on the ground. Larger bill features and short legs are associated with flycatching behavior and high, open perches. The ANCOVA reveals concordance in their ecomorphological relationships, but only in a single ecomorphological axis. The lack of complete concordance may be due to differences in habitat or broad scale historical influences between NA and SA flycatchers.     

Analysis of Sharksucker, Echeneis naucrates, Induced Behavior Patterns in the Blacktip Shark, Carcharhinus limbatus

I analyzed and quantified the behavior of blacktip sharks, Carcharhinus limbatus, irritated by sharksuckers, Echeneis naucrates, attached to their bodies. The sharksucker induced behavior patterns were divided into simple rotational patterns, expressed by body turns along their main axes (roll, yaw, pitch); and complex patterns (wiggle, shake, wind, chafe), consisting of a combination or a repetition of simple behavior patterns. Three nonrotational behavior patterns were also observed (freeze, yawn, flicker). Of the 78 blacktip sharks examined, 70 performed either a simple or a complex pattern, or a combination of the two types. Of the total 195 rotational behavior patterns observed, only three wind patterns, performed as chaffing, led to the dislocation of a sharksucker, implying that the shark's primary intention may not be to shake off the teleost, but to initiate a position change to a less sensitive part of its body. Three sharks showed behavior patterns resembling typical agonistic display patterns, but they were induced by sharksuckers, not triggered by the presence of humans.     

Learning temporal patterns of risk in a predator-diverse environment

Predation plays a major role in shaping prey behaviour. Temporal patterns of predation risk have been shown to drive daily activity and foraging patterns in prey. Yet the ability to respond to temporal patterns of predation risk in environments inhabited by highly diverse predator communities, such as rainforests and coral reefs, has received surprisingly little attention. In this study, we investigated whether juvenile marine fish, Pomacentrus moluccensis (lemon damselfish), have the ability to learn to adjust the intensity of their antipredator response to match the daily temporal patterns of predation risk they experience. Groups of lemon damselfish were exposed to one of two predictable temporal risk patterns for six days. "Morning risk" treatment prey were exposed to the odour of Cephalopholis cyanostigma (rockcod) paired with conspecific chemical alarm cues (simulating a rockcod present and feeding) during the morning, and rockcod odour only in the evening (simulating a rockcod present but not feeding). "Evening risk" treatment prey had the two stimuli presented to them in the opposite order. When tested individually for their response to rockcod odour alone, lemon damselfish from the morning risk treatment responded with a greater antipredator response intensity in the morning than in the evening. In contrast, those lemon damselfish previously exposed to the evening risk treatment subsequently responded with a greater antipredator response when tested in the evening. The results of this experiment demonstrate that P. moluccensis have the ability to learn temporal patterns of predation risk and can adjust their foraging patterns to match the threat posed by predators at a given time of day. Our results provide the first experimental demonstration of a mechanism by which prey in a complex, multi-predator environment can learn and respond to daily patterns of predation risk.     

Tactical population movements and distributions for ideally motivated competitors

The spatial distributions of populations are a reflection of underlying rules for movement behavior in the context of the environment encountered by individuals. Here I study how ideal directed movement--in which individuals travel in the direction offering the most immediate perceived improvement to their personal fitness--dictates the spatial position of two populations occupying the same relative niche and engaged in competition via interference to an individual's ability to gather resources. Drawing on the analytic derivation of equilibria, numerical simulations, and graphical assessments, I provide conditions under which sympatry, parapatry, or regional exclusion is expected during different phases of the community's development. I also demonstrate that specific competitive asymmetries produce distinguishable distributions and invasion patterns and identify which populations are found centrally or peripherally. Dynamic and dispersal equilibria were examined for differences in the sensitivity to spatial variations in fitness, per capita mortality, metabolic efficiency, the strength of interspecific interference, resource collection speed, and the optimal location of each population along an environmental cline. These asymmetries were studied both in isolation and pairwise in fitness trade-off scenarios.     

Correlations between Ontogenetic Change in Color Pattern and Antipredator Behavior in the Racer, Coluber constrictor

Differences in snake color pattern have been demonstrated to affect behaviors involved in antipredator defense. Snakes with blotched or banded color patterns are concealed when not moving, and tend to rely on concealment and aggression for defense. In contrast, snakes with uniform or striped color patterns are easily seen when stationary, but their speed and direction are difficult to track when moving. They tend to rely on flight for protection. Some snake taxa exhibit ontogenetic change in color pattern, but the behavioral consequences of this change have not been investigated. I present results of a behavioral study in the racer, Coluber constrictor, which has a blotched juvenile color pattern but is uniformly colored as an adult. Hatchling racers were significantly more likely than adults to show aggressive behavior when confronted with a model predator, whereas adults were more likely to flee. This supports the hypothesis that changes in behavior and color pattern are correlated in this species to provide effective antipredator defense at different stages of life history. I also examined sprint speed, which may be an important factor in antipredator defense. Juvenile and adult racers showed a similar relationship between length and speed, a pattern also seen in other species that lack color change. This result suggests that sprint speed is not a causal factor in the evolution of ontogenetic color change.     

Maximum Parsimony on Phylogenetic networks

Background

Phylogenetic networks are generalizations of phylogenetic trees, that are used to model evolutionary events in various contexts. Several different methods and criteria have been introduced for reconstructing phylogenetic trees. Maximum Parsimony is a character-based approach that infers a phylogenetic tree by minimizing the total number of evolutionary steps required to explain a given set of data assigned on the leaves. Exact solutions for optimizing parsimony scores on phylogenetic trees have been introduced in the past.

Results

In this paper, we define the parsimony score on networks as the sum of the substitution costs along all the edges of the network; and show that certain well-known algorithms that calculate the optimum parsimony score on trees, such as Sankoff and Fitch algorithms extend naturally for networks, barring conflicting assignments at the reticulate vertices. We provide heuristics for finding the optimum parsimony scores on networks. Our algorithms can be applied for any cost matrix that may contain unequal substitution costs of transforming between different characters along different edges of the network. We analyzed this for experimental data on 10 leaves or fewer with at most 2 reticulations and found that for almost all networks, the bounds returned by the heuristics matched with the exhaustively determined optimum parsimony scores.

Conclusion

The parsimony score we define here does not directly reflect the cost of the best tree in the network that displays the evolution of the character. However, when searching for the most parsimonious network that describes a collection of characters, it becomes necessary to add additional cost considerations to prefer simpler structures, such as trees over networks. The parsimony score on a network that we describe here takes into account the substitution costs along the additional edges incident on each reticulate vertex, in addition to the substitution costs along the other edges which are common to all the branching patterns introduced by the reticulate vertices. Thus the score contains an in-built cost for the number of reticulate vertices in the network, and would provide a criterion that is comparable among all networks. Although the problem of finding the parsimony score on the network is believed to be computationally hard to solve, heuristics such as the ones described here would be beneficial in our efforts to find a most parsimonious network.     

Ritual, Risk, and Danger: Chain Prayers in Fiji

Rituals that defuse immediate senses of danger can perpetuate senses of powerlessness. Ambiguous language used in defensive rituals can heighten people's senses of the risks they are confronting and also compel people to perform those rituals again in the future. In this article, I illustrate this argument by examining Fijian Methodist masu sema (chain prayers), which are conducted to defuse the dangers that beset society, including curses from demonic ancestors. I argue that Fijian cultural themes of present-day human powerlessness are generated largely by competition between Methodist and chiefly authorities. "Chain prayers" are attempts to negate the power of dangerous ancestors, but in requesting God's help, ritual participants cast themselves as powerless. Verbal ambiguity in chain prayers gives "demons" lives of their own, compelling their future circulation.     

Simple heuristics and rules of thumb: where psychologists and behavioural biologists might meet

The Centre for Adaptive Behaviour and Cognition (ABC) has hypothesised that much human decision-making can be described by simple algorithmic process models (heuristics). This paper explains this approach and relates it to research in biology on rules of thumb, which we also review. As an example of a simple heuristic, consider the lexicographic strategy of Take The Best for choosing between two alternatives: cues are searched in turn until one discriminates, then search stops and all other cues are ignored. Heuristics consist of building blocks, and building blocks exploit evolved or learned abilities such as recognition memory; it is the complexity of these abilities that allows the heuristics to be simple. Simple heuristics have an advantage in making decisions fast and with little information, and in avoiding overfitting. Furthermore, humans are observed to use simple heuristics. Simulations show that the statistical structures of different environments affect which heuristics perform better, a relationship referred to as ecological rationality. We contrast ecological rationality with the stronger claim of adaptation. Rules of thumb from biology provide clearer examples of adaptation because animals can be studied in the environments in which they evolved. The range of examples is also much more diverse. To investigate them, biologists have sometimes used similar simulation techniques to ABC, but many examples depend on empirically driven approaches. ABC's theoretical framework can be useful in connecting some of these examples, particularly the scattered literature on how information from different cues is integrated. Optimality modelling is usually used to explain less detailed aspects of behaviour but might more often be redirected to investigate rules of thumb.