Evolutionary mechanisms in behaviour: An intraspecific genetic approach

The study of the evolutionary mechanisms in behaviour and of the biological grounds of individual variability may be based on the comparative phylogenetic approach or on an intraspecific genetic analysis. The discontinuous behavioural progression evident across species is due to the assumption that the phylogenetic “scale” may be adopted in place of the phylogenetic trees and to the fact that today's existing species have evolved in parallel and may not be used to represent an evolutionary sequence. However, despite the existence of different motor and perceptual abilities the comparative approach has shown that many analogies exist between some basic brain mechanisms across species.The existence of outstanding individual differences within the same species must be regarded as a powerful potential tool since quantitative differences between the behaviours of different individuals belonging to the same species might later result in qualitatively different phenotypes. By using different strains and mutations of mice and different genetic approaches it has been possible to assess the mode of inheritance, to calculate estimates of heritability and of the number of segregating units for different behavioural traits ranging from avoidance to maze learning and activity. The existence of clear genetic correlations between some of these behavioural patterns has also allowed the identification of some single-gene mutants affecting these traits and the characterization of a gene responsible for a major effect on activity. This psychogenetic approach shows that there are behaviour differences which are the products of evolutionary adaptive processes and that the knowledge of the genetic systems that underlie these differences is a basic step for understanding the brain mechanisms in Man.     

Interspecies differences of motor units properties in the medial gastrocnemius muscle of cat and rat

The purpose of the study was to analyze the interspecies differences of motor unit contractile properties in two most frequently studied mammals: cats and rats. A total sample of 166 motor units (79 in cats and 85 in rats) was investigated in the medial gastrocnemius muscle. Considerable differences were found in composition of the studied muscle. In cats, fast fatigable, fast resistant and slow units formed 68, 18 and 14% of the investigated population, whereas in rats 36, 52 and 12%, respectively. The contraction and relaxation times of motor units in the cat muscle were evidently longer than in the rat and the border values for fast/slow motor units division in these species were 44 and 20 ms, respectively. The mean values of twitch and tetanic forces appeared to be 7-8 times lower in rats, for fast, while 2-5 times for slow motor units. Also variability between the strongest and the weakest units within each type revealed differences 10-60 times in cats, whereas only 3.5-14 times in rats. The summation of twitches into tetanus for fast units was comparable in both species, but for S units was evidently more effective in the cat. In fast motor units' tetanic contractions evident interspecies differences concerned sag appearance and profiles of unfused tetani of FF and FR units. Differences in contractile properties described in the study may depend on the size, number and innervation ratio of motor units in the muscle of cat and rat, as well as their biochemical variability. Differences in composition of motor unit types and uneven mechanisms of force development may reflect biological adaptation to variable behaviour of cats and rats.     

Inspiring song: The role of respiratory circuitry in the evolution of vertebrate vocal behavior

Vocalization is a common means of communication across vertebrates, but the evolutionary origins of the neural circuits controlling these behaviors are not clear. Peripheral mechanisms of sound production vary widely: fish produce sounds with a swimbladder or pectoral fins; amphibians, reptiles, and mammalians vocalize using a larynx; birds vocalize with a syrinx. Despite the diversity of vocal effectors across taxa, there are many similarities in the neural circuits underlying the control of these organs. Do similarities in vocal circuit structure and function indicate that vocal behaviors first arose in a single common ancestor, or have similar neural circuits arisen independently multiple times during evolution? In this review, we describe the hindbrain circuits that are involved in vocal production across vertebrates. Given that vocalization depends on respiration in most tetrapods, it is not surprising that vocal and respiratory hindbrain circuits across distantly related species are anatomically intermingled and functionally linked. Such vocal‐respiratory circuit integration supports the hypothesis that vocal evolution involved the expansion and functional diversification of breathing circuits. Recent phylogenetic analyses, however, suggest vocal behaviors arose independently in all major tetrapod clades, indicating that similarities in vocal control circuits are the result of repeated co‐options of respiratory circuits in each lineage. It is currently unknown whether vocal circuits across taxa are made up of homologous neurons, or whether vocal neurons in each lineage arose from developmentally and evolutionarily distinct progenitors. Integrative comparative studies of vocal neurons across brain regions and taxa will be required to distinguish between these two scenarios.     

Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutta)

The basis for our knowledge of brain evolution in vertebrates rests heavily on empirical evidence from comparative studies at the species level. However, little is still known about the natural levels of variation and the evolutionary causes of differences in brain size and brain structure within‐species, even though selection at this level is an important initial generator of macroevolutionary patterns across species. Here, we examine how early life‐history decisions and sex are related to brain size and brain structure in wild populations using the existing natural variation in mating strategies among wild brown trout (Salmo trutta). By comparing the brains of precocious fish that remain in the river and sexually mature at a small size with those of migratory fish that migrate to the sea and sexually mature at a much larger size, we show, for the first time in any vertebrate, strong differences in relative brain size and brain structure across mating strategies. Precocious fish have larger brain size (when controlling for body size) but migratory fish have a larger cerebellum, the structure in charge of motor coordination. Moreover, we demonstrate sex‐specific differences in brain structure as female precocious fish have a larger brain than male precocious fish while males of both strategies have a larger telencephalon, the cognitive control centre, than females. The differences in brain size and structure across mating strategies and sexes thus suggest the possibility for fine scale adaptive evolution of the vertebrate brain in relation to different life histories.     

How muscles accommodate movement in different physical environments: aquatic vs. terrestrial locomotion in vertebrates.

Representatives of nearly all vertebrate classes are capable of coordinated movement through aquatic and terrestrial environments. Though there are good data from a variety of species on basic patterns of muscle recruitment during locomotion in a single environment, we know much less about how vertebrates use the same musculoskeletal structures to accommodate locomotion in physically distinct environments. To address this issue, we have gathered data from a broad range of vertebrates that move successfully through water and across land, including eels, toads, turtles and rats. Using high-speed video in combination with electromyography and sonomicrometry, we have quantified and compared the activity and strain of individual muscles and the movements they generate during aquatic vs. terrestrial locomotion. In each focal species, transitions in environment consistently elicit alterations in motor output by major locomotor muscles, including changes in the intensity and duration of muscle activity and shifts in the timing of activity with respect to muscle length change. In many cases, these alterations likely change the functional roles played by muscles between aquatic and terrestrial locomotion. Thus, a variety of forms of motor plasticity appear to underlie the ability of many species to move successfully through different physical environments and produce diverse behaviors in nature.     

Integrative focus on dynamic motor patterns and age hierarchy in the expression of aggression

In this study, we analyzed the dynamic motor patterns of attack or defense and age hierarchy to investigate aggression in African mole-rats Cryptomys foxi and the house mouse Mus musculus. The objective is to verify if the social order of dominance is associated with age hierarchy within the social group. Using the resident-intruder experimental model, we created a series of dyadic encounters that comprised of a standard adult mouse or rat paired with groups of aggressive and hierarchically age-ranked small animals in a territorial aggression test. Our results indicate that though the adult animals displayed the highest level of aggression, indicating their dominant status, there was no age-related hierarchical formation in the expression of aggression. In the non-territorial aggression test in which rats or mice were grouped together, animals displayed low levels of aggression compared to the territorial test and no hierarchical age-related order. These results indicate that the magnitude of aggression expressed by animals in the social group, based on their motor patterns of attack and defense, seem to depend on individual competitive strategies in reaction to various environmental challenges and not necessarily on age hierarchy.     

Sperm competition and sperm midpiece size: no consistent pattern in passerine birds

Sperm competition is thought to be a major force driving the evolution of sperm shape and function. However, previous studies investigating the relationship between the risk of sperm competition and sperm morphometry revealed inconclusive results and marked differences between taxonomic groups. In a comparative study of two families of passerines (Fringillidae and Sylviidae) and also across species belonging to different passerine families, we investigated the relative importance of the phylogenetic background on the relationship between sperm morphometry and the risk of sperm competition. The risk of sperm competition was inferred from relative testis mass as an indicator of investment in sperm production. We found: (i) a significant positive association between both midpiece length and flagellum length and relative testis mass in the Fringillidae, (ii) a significant negative association between sperm trait dimensions and relative testis mass in the Sylviidae, and (iii) no association across all species. Despite the striking difference in the patterns shown by the Sylviidae and the Fringillidae, the relationship between midpiece length and flagellum length was positive in both families and across all species with positive allometry. Reasons for the differences and similarities between passerine families are discussed.     

Development and diversity of lignin patterns

Different patterns of lignified cell walls are associated with diverse functions in a variety of plant tissues. These functions rely on the stiffness and hydrophobicity that lignin polymers impart to the cell wall. The precise pattern of subcellular lignin deposition is critical for the structure–function relationship in each lignified cell type. Here, we describe the role of xylem vessels as water pipes, Casparian strips as apoplastic barriers, and the role of asymmetrically lignified endocarp b cells in exploding seed pods. We highlight similarities and differences in the genetic mechanisms underpinning local lignin deposition in these diverse cell types. By bringing together examples from different developmental contexts and different plant species, we propose that comparative approaches can benefit our understanding of lignin patterning mechanisms.

Diverse lignin patterns underpin distinct functions in different plant tissues.     

Comparative endocrinology of domestic and nondomestic felids

The ability to track gonadal and adrenal activity via hormones is key to optimizing health and reproduction. Through decades of study, a great deal has been learned about the biology of female domestic cats, including endocrine function. More recently, comparative endocrine studies have greatly expanded our knowledge base of nondomestic felids as well. The latter has been possible largely through the development of noninvasive fecal steroid metabolite analysis techniques, which currently is the method of choice for monitoring endocrine function in wildlife species, including felids. It now is well-recognized that a range in endocrine patterns exists among Felidae, with many traits and mechanisms being uncommon, if not unique. There is a high degree of variability in the type of ovulation (spontaneous versus induced) expressed across the taxon. Even within species, some individuals exhibit ovulation that is only induced, whereas others ovulate spontaneously as well. Steroid metabolism also differs in that metabolites are excreted almost exclusively in feces, with very little steroid found in urine. Across species there are marked differences in seasonal and social influences on reproduction, adrenal responses to husbandry practices, and ovarian responses to assisted reproductive procedures. This means that developing strategies to improve health and reproduction of felids must be done on a species by species basis. This paper summarizes current knowledge on the reproductive endocrinology of female domestic and nondomestic cats, and describes how the rapidly growing endocrine database is aiding ex situ management efforts.     

New faces in plant innate immunity: heterotrimeric G proteins

Co-existence of species seems to inevitably result in origin of parasitism and hence development of molecular mechanisms of attack and defense. Certain similarities between plant and animal defense systems point to an ancient inheritance of the innate immunity. Heterotrimeric G proteins are structurally conserved signaling molecules connecting plasma membrane bound receptors to cytoplasmic effectors. They were found in most eukaryotic organisms. Their role in human pathophysiology and animal diseases was well established. In plants these proteins were also recently implicated in innate immunity. However, molecular mechanisms governed by G proteins and providing resistance against plant pathogens seem to be different from those in animal systems and largely remain elusive. In this review we attempted to sketch current ideas of plant defense system and to present a contemporary status of heterotrimeric G proteins in plant innate immunity.     

The evolution of feeding motor patterns in vertebrates

Despite considerable skepticism, researchers have found that the patterns of muscle activation that control feeding behaviors of lower vertebrates have been surprisingly conserved during evolution. This tendency for conservation among taxa appears in the face of marked flexibility of motor patterns within individuals. One interpretation of these apparently conflicting trends is that the most effective motor pattern for any given feeding situation is the same across substantial phylogenetic distances and morphological differences. The novel evolutionary insight provided by this research is that historical changes to motor patterns are a relatively infrequent source of trophic innovation. The spectacular diversity of feeding abilities and feeding ecology in lower vertebrates is based mostly on axes of variation, and on the innovations in the organization of muscles and the skeletal linkage systems that they drive.     

Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity

Sexual dichromatism, a form of sexual dimorphism in which males and females differ in colour, is widespread in animals but has been predominantly studied in birds, fishes and butterflies. Moreover, although there are several proposed evolutionary mechanisms for sexual dichromatism in vertebrates, few studies have examined this phenomenon outside the context of sexual selection. Here, we describe unexpectedly high diversity of sexual dichromatism in frogs and create a comparative framework to guide future analyses of the evolution of these sexual colour differences. We review what is known about evolution of colour dimorphism in frogs, highlight alternative mechanisms that may contribute to the evolution of sexual colour differences, and compare them to mechanisms active in other major groups of vertebrates. In frogs, sexual dichromatism can be dynamic (temporary colour change in males) or ontogenetic (permanent colour change in males or females). The degree and the duration of sexual colour differences vary greatly across lineages, and we do not detect phylogenetic signal in the distribution of this trait, therefore frogs provide an opportunity to investigate the roles of natural and sexual selection across multiple independent derivations of sexual dichromatism.     

How the insect pathogen bacteria Bacillus thuringiensis and Xenorhabdus/Photorhabdus occupy their hosts

Insects are the largest group of animals on earth. Like mammals, virus, fungi, bacteria and parasites infect them. Several tissue barriers and defense mechanisms are common for vertebrates and invertebrates. Therefore some insects, notably the fly Drosophila and the caterpillar Galleria mellonella, have been used as models to study host-pathogen interactions for several insect and mammal pathogens. They are excellent tools to identify pathogen determinants and host tissue cell responses. We focus here on the comparison of effectors used by two different groups of bacterial insect pathogens to accomplish the infection process in their lepidopteran larval host: Bacillus thuringiensis and the nematode-associated bacteria, Photorhabdus and Xenorhabdus. The comparison reveals similarities in function and expression profiles for some genes, which suggest that such factors are conserved during evolution in order to attack the tissue encountered during the infection process.     

Mammalian Sleep Dynamics: How Diverse Features Arise from a Common Physiological Framework

Mammalian sleep varies widely, ranging from frequent napping in rodents to consolidated blocks in primates and unihemispheric sleep in cetaceans. In humans, rats, mice and cats, sleep patterns are orchestrated by homeostatic and circadian drives to the sleep–wake switch, but it is not known whether this system is ubiquitous among mammals. Here, changes of just two parameters in a recent quantitative model of this switch are shown to reproduce typical sleep patterns for 17 species across 7 orders. Furthermore, the parameter variations are found to be consistent with the assumptions that homeostatic production and clearance scale as brain volume and surface area, respectively. Modeling an additional inhibitory connection between sleep-active neuronal populations on opposite sides of the brain generates unihemispheric sleep, providing a testable hypothetical mechanism for this poorly understood phenomenon. Neuromodulation of this connection alone is shown to account for the ability of fur seals to transition between bihemispheric sleep on land and unihemispheric sleep in water. Determining what aspects of mammalian sleep patterns can be explained within a single framework, and are thus universal, is essential to understanding the evolution and function of mammalian sleep. This is the first demonstration of a single model reproducing sleep patterns for multiple different species. These wide-ranging findings suggest that the core physiological mechanisms controlling sleep are common to many mammalian orders, with slight evolutionary modifications accounting for interspecies differences.     

Variation in steroid hormone levels among Caribbean Anolis lizards: Endocrine system convergence?

Variation in aggression among species can be due to a number of proximate and ultimate factors, leading to patterns of divergent and convergent evolution of behavior among even closely related species. Caribbean Anolis lizards are well known for their convergence in microhabitat use and morphology, but they also display marked convergence in social behavior and patterns of aggression. We studied 18 Anolis species across six ecomorphs on four different Caribbean islands to test four main hypotheses. We hypothesized that species differences in aggression would be due to species differences in circulating testosterone (T), a steroid hormone implicated in numerous studies across vertebrate taxa as a primary determinant of social behavior; more aggressive species were expected to have higher baseline concentrations of T and corticosterone. We further hypothesized that low-T species would increase T and corticosterone levels during a social challenge. Within three of the four island assemblages studied we found differences in T levels among species within an island that differ in aggression, but in the opposite pattern than predicted: more aggressive species had lower baseline T than the least aggressive species. The fourth island, Puerto Rico, showed the pattern of baseline T levels among species we predicted. There were no patterns of corticosterone levels among species or ecomorphs. One of the two species tested increased T in response to a social challenge, but neither species elevated corticosterone. Our results suggest that it is possible for similarities in aggression among closely related species to evolve via different proximate mechanisms.     

Complementary Models of Tree Species–Soil Relationships in Old-Growth Temperate Forests

Ecosystem-level studies identify plant–soil feedbacks as important controls on soil nutrient availability, particularly for nitrogen and phosphorus. Although site- and species-specific studies of tree species–soil relationships are relatively common, comparatively fewer studies consider multiple co-existing species in old-growth forests across a range of sites that vary in underlying soil fertility. We characterized patterns in forest floor and mineral soil nutrients associated with four common tree species across eight undisturbed old-growth forests in Oregon, USA, and used two complementary conceptual models to assess tree species–soil relationships. Plant–soil feedbacks that could reinforce site-level differences in nutrient availability were assessed using the context-dependent relationships model, whereby relative species-based differences in each soil nutrient diverged or converged as nutrient status changed across sites. Tree species–soil relationships that did not reflect strong feedbacks were evaluated using a site-independent relationships model, whereby forest floor and surface mineral soil nutrient pools differed consistently by tree species across sites, without variation in deeper mineral soils. We found that the organically cycled elements carbon, nitrogen, and phosphorus exhibited context-dependent differences among species in both forest floor and mineral soil, and most often followed a divergence model, whereby species differences were greatest at high-nutrient sites. These patterns are consistent with theory emphasizing biotic control of these elements through plant–soil feedback mechanisms. Site-independent species differences were strongest for pools of the weatherable cations calcium, magnesium, potassium, as well as phosphorus, in mineral soils. Site-independent species differences in forest floor nutrients were attributable to one species that displayed significantly greater forest floor mass accumulation. Our findings confirm that site-independent and context-dependent tree species-soil relationships occur simultaneously in old-growth temperate forests, with context-dependent relationships strongest for organically cycled elements, and site-independent relationships strongest for weatherable elements with inorganic cycling phases. These models provide complementary explanations for patterns of nutrient accumulation and cycling in mixed-species old-growth temperate forests.     

A global review of the impacts of invasive cats on island endangered vertebrates

Cats are generalist predators that have been widely introduced to the world's ~179 000 islands. Once introduced to islands, cats prey on a variety of native species many of which lack evolved defenses against mammalian predators and can suffer severe population declines and even extinction. As islands house a disproportionate share of terrestrial biodiversity, the impacts of invasive cats on islands may have significant biodiversity impacts. Much of this threatened biodiversity can be protected by eradicating cats from islands. Information on the relative impacts of cats on different native species in different types of island ecosystems can increase the efficiency of this conservation tool. We reviewed feral cat impacts on native island vertebrates. Impacts of feral cats on vertebrates have been reported from at least 120 different islands on at least 175 vertebrates (25 reptiles, 123 birds, and 27 mammals), many of which are listed by the International Union for the Conservation of Nature. A meta‐analysis suggests that cat impacts were greatest on endemic species, particularly mammals and greater when non‐native prey species were also introduced. Feral cats on islands are responsible for at least 14% global bird, mammal, and reptile extinctions and are the principal threat to almost 8% of critically endangered birds, mammals, and reptiles.     

The geography of diet variation in Neotropical Carnivora

1. Mammalian carnivores (order Carnivora) perform important regulatory functions in terrestrial food webs. Building a comprehensive knowledge of the dietary patterns of carnivorans and the factors determining such patterns is essential for improving our understanding of the role of carnivorans in ecosystem functioning.
2. In the Neotropics, there are 64 extant species of terrestrial Carnivora, but information on their trophic ecology is diffuse. We compiled and analysed the available quantitative dietary data for Neotropical carnivorans, aiming to detect patterns of intraspecific and interspecific dietary variation at a large geographical scale.
3. The resulting database encompasses information on trophic interactions of 37 native carnivoran species from six families across 14 countries. There are clear geographical biases towards southern Brazil, Chile, and Argentina, and a noticeable knowledge gap within the Amazon. Also, most studies are focused on canids and felids, especially Puma concolor, Panthera onca, Cerdocyon thous, Leopardus pardalis, and Chrysocyon brachyurus, whereas for 27 native species, we found no quantitative dietary information.
4. Neotropical carnivorans consume species from at least 651 genera of vertebrates, invertebrates, and plants. We found clear species-specific dietary patterns and marked differences between Neotropical felids and canids. Although predators generally exhibit high levels of consistency in their diets regarding prey body mass, we detected significant intraspecific variation for all species analysed across study sites.
5. Body mass imposes strong constraints on prey use, but biogeographical differences in prey availability and human influence may drive the geographical variation we found. Overall, observed patterns show not only similarities with resource-use patterns found for carnivorans in other continents, such as nestedness driven by body mass, but also differences, such as high levels of frugivory and consumption of invertebrates by canids. Assessing resource-use patterns is the first step towards a better understanding of processes underlying the organisation of trophic interactions, and is imperative for addressing impacts of defaunation on ecosystems and for informing conservation efforts.

     

Modular Evolution of PGC-1α in Vertebrates

In mammals, the peroxisome proliferator activated receptor (PPAR)γ coactivator-1α (PGC-1α) is a central regulator of mitochondrial gene expression, acting in concert with nuclear respiratory factor-1 (NRF-1) and the PPARs. Its role as a “master regulator” of oxidative capacity is clear in mammals, but its role in other vertebrates is ambiguous. In lower vertebrates, although PGC-1α seems to play a role in coordinating the PPARα axis as in mammals, it does not appear to be involved in NRF-1 regulation of mitochondrial content. To evaluate the evolutionary patterns of this coactivator in fish and mammals, we investigated the evolutionary trajectories of PGC-1α homologs in representative vertebrate lineages. A phylogeny of the PGC-1 paralogs suggested that the family diversified through repeated genome duplication events early in vertebrate evolution. Bayesian and maximum likelihood phylogenetic reconstructions of PGC-1α in representative vertebrate species revealed divergent evolutionary dynamics across the different functional domains of the protein. Specifically, PGC-1α exhibited strong conservation of the activation/PPAR interaction domain across vertebrates, whereas the NRF-1 and MEF2c interaction domains experienced accelerated rates of evolution in actinopterygian (fish lineages) compared to sarcopterygians (tetrapod lineages). Furthermore, analysis of the amino acid sequence of these variable domains revealed successive serine- and glutamine-rich insertions within the teleost lineages, with important ramifications for PGC-1α function in these lineages. Collectively, these results suggest modular evolution of the PGC-1α protein in vertebrates that could allow for lineage-specific divergences in the coactivating capabilities of this regulator.