Comprehensive Study Guide on Behavioral Ecology and Evolutionary Ecology

Overview of Behavioral Ecology

Humans have observed and studied animal behavior for as long as they have populated the Earth. In our early history as both hunter and prey, a deep understanding of animal behavior was vital for human survival and decision-making. In the modern era, behavioral ecology has developed as a scientific discipline that investigates how behavior develops, how it evolves over time, and the specific ways it contributes to an organism's survival and reproductive success.

Proximate and Ultimate Causes of Behavior

Behavioral ecologists distinguish between two primary classes of scientific questions regarding behavior: proximate and ultimate causes. Behavior itself is defined broadly as everything an animal does and the manner in which it performs those actions. This includes muscular activities, such as a predator chasing its prey or a bird singing a complex song, as well as non-muscular activities, like an animal secreting a pheromone to attract a mate. Learning is also categorized as a behavioral process. Behavioral traits are considered an essential component of an animal’s phenotype.

Proximate questions are mechanistic in nature. They focus on the "how" of a behavior, examining the environmental stimuli that trigger an act, alongside the genetic, physiological, and anatomical mechanisms that underly it. For example, a proximate question regarding the breeding of red-crowned cranes might ask how day length influences their reproductive timing. A potential proximate hypothesis suggests that increasing day length in spring triggers the production of and response to specific hormones, which then initiates breeding behavior.

Ultimate questions address the evolutionary significance of a behavior, focusing on the "why" behind it. These questions explore why natural selection favors a specific behavior in terms of its contribution to survival and reproduction. Regarding the red-crowned crane, an ultimate hypothesis would posit that these birds breed in the spring because that is when food supplies are most abundant. This abundance provides an advantage in reproductive success by allowing parents to find ample food for rapidly growing offspring. These two levels of causation are intrinsically linked, as proximate mechanisms produce the behaviors that have evolved because they increase an organism's overall fitness.

Genetic Components of Behavior

Behavior is the result of complex interactions between genetic factors and environmental influences. The nature-versus-nurture debate in biology focuses on how both genes and the environment are involved in behavior, rather than suggesting one excludes the other. Behavior can be viewed through the lens of the norm of reaction, which measures the behavioral phenotypes for a specific genotype across a range of environments. While some behaviors are highly variable based on experience, others are developmentally fixed and are known as innate behaviors. These innate behaviors are under strong genetic influence and remain consistent despite environmental differences.

Many animal movements demonstrate substantial genetic influence. A kinesis is a simple change in activity or turning rate in response to a stimulus. For instance, sowbugs are more active in dry areas and less active in humid ones, increasing their chances of finding moisture. A taxis is an automatic, oriented movement toward or away from a stimulus. Stream fishes exhibit positive rheotaxis, automatically orienting themselves upstream to face the current, which prevents them from being swept away and positions them to catch incoming food.

Migratory behavior is also often genetically programmed. Migration refers to the regular movement of animals over relatively long distances. In blackcaps ($Sylvia atricapilla$), a warbler ranging from the Cape Verde Islands to northern Europe, migratory restlessness is a known genetic trait. Peter Berthold conducted studies where migratory blackcaps were crossed with non-migratory ones. In the resulting offspring, $40\%$ showed migratory restlessness regardless of the environment they were raised in, suggesting that migration follows a polygenic inheritance pattern.

Animal Communication and Signals

Social interactions between animals rely heavily on signals, which are behaviors that cause a change in the behavior of another animal. Animal communication involves the transmission, reception, and response to these signals. While the environment contributes to communication systems, many signals are under strong genetic control. Signals are often energy-efficient; for example, a territorial fish may simply erect its fins to ward off an intruder rather than expending more energy on a physical attack.

Animals use visual, auditory, chemical, tactile, and electrical signals depending on their lifestyle and environment. Nocturnal species frequently utilize olfactory and auditory signals, whereas diurnal birds, which often have a poor sense of smell, rely on visual and auditory communication. Chemical substances called pheromones are especially common in mammals and insects for reproductive and non-reproductive purposes. In honeybees, pheromones maintain social order in the hive, attracting drones to the queen. In minnows, an alarm substance released from an injured fish's skin induces a fright response and schooling behavior in others. These pheromones are effective even at very low concentrations.

Insect mating rituals often include songs under direct genetic control. In $Drosophila$, males vibrate their wings to produce a song that females recognize. Males raised in isolation produce the same characteristic song as those raised with others, showing little variation. In some cases, morphologically identical species, such as green lacewings, can only be identified by their unique courtship songs. There are at least $15$ different species of lacewings identified this way, and hybrid offspring produce songs containing elements of both parental species, confirming genetic control.

Genetic Influence on Mating and Parental Behavior

In prairie voles ($Microtus ochrogaster$), mating and parental behaviors are under strong genetic influence. Unlike $97\%$ of mammalian species, prairie voles are monogamous. After mating, males form strong pair-bonds, help care for young, and become intensely aggressive toward strangers while remaining non-aggressive toward their mate and pups. Research at Emory University by Thomas Insel showed that arginine-vasopressin (AVP), a nine-amino-acid neurotransmitter released during mating, mediates these behaviors by binding to V1a receptors in the central nervous system.

There are significant differences in the distribution of V1a receptors between monogamous prairie voles and promiscuous montane voles. When the prairie vole V1a receptor gene was inserted into laboratory mice, the mice developed the same receptor distribution and displayed similar mating behaviors. This indicates that a single gene can mediate complex mating and parental behaviors.

Environmental Influences and Learning

Environmental factors can modify behavior significantly. For instance, the diet of $Drosophila mojavensis$ larvae influences mate selection in adults. Females prefer males raised on the same cactus species they were raised on, assessing them via taste based on hydrocarbons in the exoskeleton. Similarly, cross-fostering experiments between California mice ($Peromyscus californicus$), which are monogamous and aggressive, and white-footed mice, which are not, showed behavioral changes. California mice raised by white-footed parents became less aggressive and provided less care, while white-footed mice raised by California parents became more aggressive.

Learning is the modification of behavior based on specific experiences and ranges from simple to complex. Habituation is a simple form of learning where an animal stops responding to unimportant stimuli, such as a warning signal not followed by an actual attack (the "cry wolf" effect). Ultimate causation explains habituation as a way to increase fitness by focusing energy on meaningful stimuli.

Spatial learning allows animals to modify behavior based on the structural layout of their environment, including the location of food and nests. Niko Tinbergen demonstrated that digger wasps use stable landmarks to find their nest entrances. Environmental variability dictates learning strategies; for example, sticklebacks from unstable river environments learn mazes via movement patterns, while those from stable ponds use a combination of movements and landmarks. Some animals, such as corvids (crows, ravens, jays), form cognitive maps, which are internal codes of spatial relationships. Pinyon jays can keep track of location and food quality for as many as a thousand different food caches.

Associative Learning and Cognition

Associative learning is the ability to connect one stimulus with another. Classical conditioning is a type of associative learning, such as when $Drosophila melanogaster$ is trained to avoid an odor paired with an electrical shock. In nature, zebra fish can learn to associate the odor of a predatory pike with an alarm substance, even if they have no innate fear of the pike. Operant conditioning, or trial-and-error learning, occurs when an animal associates its own behavior with a reward or punishment, such as a mouse learning to avoid a poisonous, brightly colored caterpillar.

Cognition, in a broad sense, is the ability of an animal's nervous system to perceive, store, process, and use sensory information. Cognitive ethology studies the connection between the nervous system and behavior. Many animals can categorize objects as "same" or "different." Primates, dolphins, and corvids are known for novel problem-solving behavior. This can occur through individual trial or by observing others, such as chimpanzees learning to solve problems by copying their peers.

Complex behaviors like bird songs involve both genetic and environmental factors. Some species, like New World flycatchers, sing their species-specific song even if raised in isolation. Others, like white-crowned sparrows, have a sensitive period where they must hear the song of their species to develop it normally later. This is followed by a subsong phase where the juvenile compares its own singing to the memorized template. Canaries exhibit a yearly plastic song stage where they can learn new song "syllables."

Evolutionary Selection of Behavioral Traits

Natural selection results in the evolution of behavioral traits because genes influence behavior. Behavioral variation within a species often corresponds to different environmental conditions. A classic example is the garter snake ($Thamnophis elegans$). Coastal populations primarily eat slugs, while inland populations do not. Research by Stevan Arnold showed that $73\%$ of newborn coastal snakes attacked slugs, compared to only $35\%$ of inland snakes. This behavior evolved approximately $10,000$ years ago when inland snakes colonized coastal areas and those able to recognize slugs via chemoreception had higher fitness.

In the funnel web spider ($Agelenopsis aperta$), spiders in food-poor arid habitats are more aggressive and return to foraging faster after a disturbance than those in riparian forests. This aggressiveness is genetic. In riparian zones, the high density of bird predators selects for more timid spider behavior due to predation risk.

Laboratory experiments on organisms with short lifespans provide evidence for behavioral evolution. Marla Sokolowski studied the $for$ gene in $Drosophila melanogaster$, which has two alleles: $for^R$ (rover phenotype) and $for^S$ (sitter phenotype). In high-density populations, the rover allele increased because long-distance foraging was necessary to find food. In low-density populations, the sitter allele increased as short-distance foraging was sufficient. Additionally, blackcap migration patterns in Germany have shifted rapidly over the last $50$ years. Traditionally, none migrated west to Britain, but by the $1990s$, $7-11\%$ of the population did so, benefiting from Britain’s milder winters and bird feeders.

Foraging Behavior and Optimal Foraging Theory

Foraging includes the mechanisms used to recognize, search for, and capture food. Optimal foraging theory suggests that foraging behavior is a compromise between the benefits of nutrition and the costs of obtaining it, such as energy use and predation risk. Natural selection favors strategies that minimize costs and maximize benefits. Reta Zach showed that crows drop whelks from an average height that balances the energy spent flying with the energy needed to break the shell.

Bluegill sunfish choose prey relative to density. At high densities, they select only large $Daphnia$ to maximize energy. At low densities, they become less selective. Younger fish are often less efficient at this, possibly due to underdeveloped vision or a lack of learning. Predation risk also dictates foraging; mule deer in Idaho avoid forest edges and interiors where mountain lions are most likely to kill them, preferring to forage in open areas while constantly scanning their surroundings.

Mating Systems and Sexual Selection

Social mating relationships vary and include promiscuous (no lasting bonds), monogamous (one male, one female), and polygamous (one individual with multiple partners). Polygamy is further divided into polygyny (one male, many females) and polyandry (one female, many males). Monogamous species are usually morphologically similar, while polygynous species are dimorphic with showy males, and polyandrous species feature ornamented females.

Parental investment, the time and resources spent raising offspring, constrains these systems. Most birds are monogamous because hatchlings require a continuous food supply that two parents can better provide. In contrast, birds with young that can feed themselves, like quail, are often polygynous. In mammals, the female is often the sole provider due to lactation, though males may provide protection. Certainty of paternity also influences investment. It is lower in internal fertilization where mating and birth are separated, but higher in external fertilization ($69\%$ of families compared to $7\%$ in internal fertilization), as egg laying and mating occur together.

Sexual selection results in sexual dimorphism. Intersexual selection involves mate choice, such as female zebra finches preferring males with red feathers if they were raised by an ornamented father. Stalk-eyed fly females prefer males with long eyestalks, which correlate with health and genetic quality. Intrasexual selection involves competition, often through ritualized agonistic behaviors. In the marine isopod ($Paracerceis sculpta$), three male types exist: alpha (defend harems), beta (female mimics), and gamma (tiny sneakers). Their success depends on harem size and density, resulting in approximately equal mating success for all three types over time.

Game theory evaluates strategies where the outcome depends on the actions of others. In side-blotched lizards ($Uta stansburiana$), three male throat colors (orange, blue, yellow) represent different strategies. Orange males are aggressive and territorial, blue males defend smaller territories, and yellow males are sneaky mimics. Their success is cyclical: blue-throats can defend against yellow-throats but lose to orange-throats; orange-throats take territories from blue-throats but lose females to sneaky yellow-throats; and yellow-throats thrive until blue-throats become more abundant again.

Inclusive Fitness and Altruism

Altruism is behavior that decreases an individual's fitness while increasing the fitness of others. Examples include Belding’s ground squirrels giving alarm calls, sterile honeybee workers defending a hive, and non-reproductive naked mole rats caring for a queen and kings. These behaviors are maintained through inclusive fitness, which is the total effect an individual has on proliferating its own genes by reproducing and by helping relatives. William Hamilton proposed Hamilton’s Rule for predicting altruism: $rB > C$, where $B$ is the benefit to the recipient, $C$ is the cost to the altruist, and $r$ is the coefficient of relatedness. Kin selection is the mechanism through which inclusive fitness operates.

Reciprocal altruism occurs between unrelated individuals if the favor is likely to be returned. This is common in stable social groups where "cheaters" face social consequences. Behavioral ecologists use the "tit for tat" strategy from game theory to explain this: an individual is cooperative on the first encounter and then mimics the previous action of the other individual in subsequent meetings.

Social learning, or learning by observing others, forms the roots of culture. In guppies ($Poecilia reticulata$), females may copy the mate choices of others, sometimes overriding their genetic preference for orange males. Vervet monkeys ($Cercopithecus aethiops$) learn to improve the accuracy of their complex alarm calls for leopards, eagles, and snakes by observing adults and receiving social confirmation. Sociobiology, as described by E. O. Wilson in $1975$, suggests that social behaviors are expressions of genes favored by natural selection. While genes influence the spectrum of human behavior, our capacity for learning and the creation of complex cultural institutions like laws and religions make human behavior uniquely plastic.